Heliothis Management

International Workshop on Heliothis Management

International Crops Research Institute for the Semi-Arid Tropics

Proceedings of the International Workshop on Heliothis Management

ICRISAT Center Patancheru, India 15-20 November 1981

International Crops Research Institute for the Semi -Arid Tropics ICRISAT Patancheru P.O. Andhra Pradesh, India 502 324 The Potential Use of Microbials in Heliothis Management M . R . B e l l 1 3 7

Possibilities for Natural Enemies in Heliothis Management D. J. Greathead and 1 4 7 and the Contribution of the Commonwealth D. J. Girling Institute of Biological Control

The Utilization of Biological Control in Heliothis Sudha Nagarkatti 1 5 9 Management in India

Discussion - Session 3 1 6 8

Session 4 - Chemical Pesticides: Their Uses and Abus e s 1 7 1

A Critical Review of the Role of Chemical R. J. V. Joyce 1 7 3 Pesticides in Heliothis Management

A Determination of an Economic Injury Level of P. H. Twine and 1 8 9 Heliothis armigera (Hubner) in Sorghum for I. R. K a y Southeast Queensland

The Likely Impact of Synthetic Pyrethroids on A . K o h l i 1 9 7 Heliothis Management

Discussion - Session 4 2 0 5

Session 5 - Host-Plant x Heliothis Interactions and 2 0 7 Resistance Screening

The Importance of Heliothis-Crop Interactions in the B. R. Wiseman 2 0 9 Management of the Pest

A Review of the Problems, Progress, and Prospects M. J. Lukefahr 2 2 3 for Host-Plant Resistance to Heliothis s p e c i e s

The Potential Role of Natural Product Chemistry M. Jacobson 2 3 3 Research in Heliothis Management

The Chemist's Role in Host-Plant Resistance Studies H. Rembold and 2 4 1 E . W i n t e r

Progress in Research on Chemical Aspects of A. C. Waiss, Jr., 2 5 1 Host-Plant Resistance to Heliothis zea in R.G.Binder, B.G.Chan, Corn, Soybean, and Tomato C. A. Elliger, and D. L. Dreyer

Techniques for Efficient Mass Rearing and J . A . M i h m 2 5 5 Infestation in Screening for Host-Plant Resistance to Corn Earworm,Heliothis zea

Screening Groundnut for Heliothis Resistance W. V. Campbell, 2 6 7 J. C. Wynne, and H. T. Stalker

Screening Legumes for Resistance to Heliothis D. J. Rogers 2 7 7

Discussion - Session 5 2 8 8

iv Session 6 - Novel Methods of Heliothis Management 2 8 9

The Present Status and Potential for Novel Uses A. N. Sparks, 2 9 1 of Pheromone to Control Heliothis J. R. Raulston, J. E. Carpenter, and P. D. Lingren

Practical Development of Pheromones in Heliothis J. R. McLaughlin and 3 0 9 M a n a g e m e n t E. R. Mitchell

Preliminary Studies on the Female G. H. L. Rothschild, 3 1 9 Sex Pheromones of Heliothis Species and A.G.L. Wilson, and Their Possible Use in Control Programs in Australia K. W. Malafant

The Potential for Hybrid Sterility in Heliothis F. I. Proshold, 3 2 9 M a n a g e m e n t M. J. Laster, D. F. Martin, and E . G . K i n g

Discussion - Session 6 3 4 0

Session 7 - Integration of Management 3 4 1

Past and Future Heliothis Management in Australia A. G. L. Wilson 3 4 3

Problems and Progress in Heliothis Management 3 5 5 B. T. Nyambo in Tanzania, with Special Reference to Cotton

Progress in Research and Development for Heliothis 3 6 3 A. N. Balla Management in the Sudan

The Problems and Prospects of Heliothis 3 6 9 G . H a r i r i Management in Southwest Asia

Progress and Problems in Heliothis Management 3 7 5 J. A. Gledhill in Tropical Southern Africa

Research on Heliothis at ICRISAT V. S. Bhatnagar, 3 8 5 S. S. Lateef, S. Sithanantham, C. S. Pawar, and W . R e e d

Discussion - Session 7 3 9 7

Session 8 - Prospects for Future International Coope r a t i o n 3 9 9

Discussions and Recommendations 4 0 1

Appendix 1 - Participants 4 1 3

V Objectives of the Workshop:

- To assemble the world's most experienced and acti ve scientists who are working on aspects of Heliothis spp management

- To review the known information

- To determine the priorities tor future action and cooperation

Organizing Committee

J.C. Davies C h a i r m a n W . R e e d Vice-Chairman Y.L. N e n e M e m b e r V.S. Bhatnagar M e m b e r S.S. Lateef M e m b e r C.S. P a w a r M e m b e r S. Sithanantham M e m b e r S. Krishnan Secretary

Acknowledgments

We wish to acknowledge the support of the many organizations who have financed the travel of participants. We are particularly grateful for generous financial support provided by the Australian Development Assistance Bureau which has enabled participants from developing countries and Australia to participate.

vi Foreword

An important function of an international research institute is to hold workshops, conferences, and symposia where delegates from many parts of the world can meet to discuss research problems and progress. ICRISAT has hosted many such workshops in the past, but this is the first in the entomological field. Heliothis s p p a r e pests of all our mandate crops—pigeonpea, chickpea, g r o u n d n u t , s o r g h u m , a n d millet—in almost all areas of the world where they are grown. Thus ICRISAT has a particularly keen interest in the management of thes e p e s t s . Much research on the management of Heliothis has been conducted on cotton, especially in the USA, Africa, and Australia, and w e are pleased to welcome several cotton entomologists from these areas to this works hop. To control Heliothis s p p o n cash crops, including cotton, insecticides have bee n used extensively and intensively, with good short-term economic returns but wi th consequent longer term problems in some areas. Most of ICRISAT's target far mers use no pesticides, partly because the economics of our mandate crops—with the possible exception of groundnut—do not permit the use of such costly inpu t s , b u t a l s o b e c a u s e t h e farmers have no access to suitable pesticides or to the means and knowledge required for their efficient application. We therefore concentrate our research upon those el e m e n t s o f Heliothis m a n - agement that are likely to be of practical value in the fields of these farmers who have limited resources. In particular, we hope to use ou r extensive germplasm resources to select and breed crops that are resistant to att a c k s b y Heliothis and other pests. However, we cannot rely entirely on a single means of pest management, so we are also studying several other elements that may be of value in the farmers' fields. This volume contains the papers that were presented by specialists on several important aspects of Heliothis management research and summaries of the discussions that followed. I was very pleased to learn th at new cooperative research initiatives were agreed upon during the workshop. I hope that these Proceedings will be of value to the many people who are concerned wi t h Heliothis management.

L.D. S w i n d a l e Director General

vii

Opening Session

Chairman: J.C. Davies

Welcome to ICRISAT and the Workshop

J.S. Kanwar and J.C. Davies*

W h i l e w e l c o m i n g t h e 5 5 participants f r o m 1 1 c o u n - Dr. D a v i e s t h e n w e l c o m e d t h e participants t o t h e tries to ICRISAT, Dr. K a n w a r outlined t h e objectives w o r k s h o p . H e outlined t h e objectives o f t h e work- of ICRISAT, t h e s e being: s h o p , w h i c h w e re :

• To s e r v e as a w o r l d center to i m p r o v e t h e y i e l d • T o a s s e m b l e t h e world's m o s t e x p e r i e n c e d a n d and nutritional quality of sorghum, pearl millet, active scientists working on various aspects of p i g e o n p e a , c h i c k p e a a n d groundnut. Heliothis spp m a n a g e m e n t . • To d e v e l o p f a r m i n g s y s t e m s w h i c h will help to • To review the known information. increase and stabilize agricultural production • To d e t e r m i n e t h e priorities for future a c t i o n a n d t h r o u g h better use of natural a n d h u m a n resour- cooperation. ces in the seasonally dry semi-arid tropics. • To identify socioeconomic and other con- H e c o m m e n t e d u p o n the excellent r e s p o n s e that straints to agricultural d e v e l o p m e n t in t h e s e m i - we h a v e h a d f r o m t h e scientists interested in Helio• arid tropics a n d to evaluate alternative m e a n s of this. Of t h o s e invited, all but a f e w h a d c o m e , d e s • alleviating them through technological and insti- pite major problems of busy schedules and tutional changes. restricted funds. Dr. D a v i e s also paid tribute to the • To assist national a n d regional r e s e a r c h pro- m a n y p e o p l e w h o h a d b e e n involved in all stages of g r a m s t h r o u g h c o o p e r a t i o n a n d support a n d t o t h e preparation a n d o p e r a t i o n of the w o r k s h o p . contribute further by sponsoring conferences, This workshop provides a unique opportunity for operating international training programs, and u s t o c o m p a r e a n d d i s c u s s t h e r e s e a r c h w o r k that assisting extension activities. has b e e n carried out on the different species of Heliothis that are p e s t s in t h e O l d a n d N e w Worlds. Dr. K a n w a r also e x p l a i n e d t h e organization a n d It also gives an opportunity for entomologists w h o structure of ICRISAT's r e s e a r c h p r o g r a m s b o t h in h a v e c o n c e n t r a t e d their r e s e a r c h u p o n single India a n d in other countries. He told t h e participants c r o p s , s u c h a s c o t t o n a n d maize, t o c o m e together that t h e ICRISAT C e n t e r f a r m is 1 3 9 4 ha, of w h i c h a n d to e x a m i n e the potential for integrating t h e 1 4 0 h a h a v e b e e n p r e s e r v e d free f r o m pesticide findings. Heliothis is being increasingly recognized use. T h e s e pesticide-free a r e a s are particularly as a broad-spectrum pest, and especially where useful for e n t o m o l o g i c a l a n d other r e s e a r c h , for agriculture is improving. they provide conditions that are c l o s e r to t h e Noting that t h e pest w a s o n e that a t t a c k s all five f a r m e r s ' conditions t h a n are normally available o n c r o p s in ICRISAT's m a n d a t e a n d that t h e s e are r e s e a r c h stations. H e also d e s c r i b e d t h e c l o s e d often g r o w n in intercrop or r e l a y - c r o p situations by s e a s o n that has b e e n a d o p t e d at ICRISAT: for 2 small farmers, Dr. Davies s t r e s s e d t h e i m p o r t a n c e m o n t h s e a c h year n o c r o p s are g r o w n o n t h e farm. of t h e e x c h a n g e of existing information to e n a b l e T h i s m e a s u r e has helped t o r e d u c e t h e pest p r o b - research priorities and strategies to be determined. l e m s a n d , c o n s e q u e n t l y , t h e pesticide use, at ICRI- H e also e m p h a s i z e d that the major benefits f r o m S A T . T h e s e a n d other m e a s u r e s w e r e c i t e d t o s u c h a w o r k s h o p c o u l d be e x p e c t e d to originate in illustrate t h e practical a p p r o a c h that t h e institute is t h e d i s c u s s i o n s a n d e x c h a n g e s of v i e w s that will t a k i n g t o w a r d s pest m a n a g e m e n t a n d t o w a r d s t a k e p l a c e b o t h within t h e s e s s i o n s a n d outside. H e e n s u r i n g that t h e r e s e a r c h c o n d u c t e d o n t h e f a r m h o p e d that initiatives w o u l d be t a k e n that w o u l d will be of u s e in our target f a r m e r s ' fields. help t h e ICRISAT scientists to a d v a n c e their Helio- this m a n a g e m e n t r e s e a r c h in c o o p e r a t i o n with t h e other participants, w h o h a v e a n e n o r m o u s r a n g e o f e x p e r i e n c e a n d expertise, a n d t o d e t e r m i n e g a p s i n *Director of Research and Director for International Cooperation, respectively, ICRISAT, Patancheru, A.P., India. k n o w l e d g e of the s p e c i e s to be defined.

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International 1 Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A P , India. Dr. Davies hoped that areas of cooperative research and collaboration between ICRISAT scientists and the scientists of developed and developing country institutions would be identified in the field of Heliothis pest management and out• lined the complex nature of some of the problems posed by the pest to small farmers of direct con• cern to ICRISAT.

2 The Nomenclature of Heliothis and Associated Taxa (Lepidoptera: Noctuidae): Past and Present

I.W.B. Nye*

Abstract

The history of the nomenclature of Heliothis, particularly of the species armigera and zea, is reviewed. From 1806, when the name Heliothis was first used, there has been continuing contusion, with several changes in both generic and specific names. The confusion is not yet fully resolved, but the author has requested the International Commission on Zoological Nomenclature to rule that the gender of the generic name H e l i o t h i s is feminine. It this request is granted, the long-accepted spellings of specific names, including armigera, will be retained.

This paper should p e r h a p s be subtitled "A T a l e of purposes resulted in controversy for many years, Great C o n f u s i o n " and, as the g e n e r i c n a m e Helio• culminating in t h e application for a ruling by t h e this a n d the specific n a m e s armigera a n d zea are International Commission on Zoological Nomen• u s e d t o d e n o t e t a x a o f s u c h i m m e n s e e c o n o m i c clature (ICZN 1926). The results of this application importance, a summary of the nomenclatural his- w e r e published in Opinion 97, t h e s u m m a r y of tory of these names is provided. w h i c h is as follows: In or about 1806, J. HUbner of A u g s b u r g , Ger- many, distributed a single quarto sheet printed on S U M M A R Y . H u bne r' s Tentamen, 1 8 0 6 , both sides, entitled Tentamen determinations was obviously prepared essentially as a digestionis atque denominationis singularum stir- manifolded manuscript, or as a proof sheet pium Lepidopterorum, peritis ad inspiciendum et (cf. Opinion 87), for examination a n d opinion dijudicandum c o m m u n i c a t u m , a J a c o b o H u b n e r . A by a restricted g r o u p of experts, i.e., in L e p i • facsimile of this rare work is provided by Hemming doptera, a n d not for general distribution as a (1937). This Tentamen p r e s e n t e d the plan of a r e c o r d in Zoology. Accordingly, the c o n c l u • classification of the L e p i d o p t e r a in w h i c h e a c h of sion that it w a s published in 1806 is subject to 107 stirpes (equivalent to present-day genera) debate. Even if t h e premise be admitted that w e r e u s e d in c o m b i n a t i o n with a single specific it w a s published in 1806, the point is debat• n a m e . T h e i m p o r t a n c e of t h e Tentamen lay in t h e able whether the contained binomials should fact that out of t h e 1 0 7 g e n e r i c n a m e s , 94 w e r e be construed as generic plus specific u s e d for t h e first time, including Heliothis. T h e n a m e s . E v e n if it be admitted that t h e b i n o m • question of w h e t h e r t h e n a m e s in t h e Tentamen ials represent combinations of generic plus w e r e to be r e g a r d e d as available for n o m e n c l a t u r a l specific names, they are essentially nomina nuda (as of t h e date in question) s i n c e authors who do not possess esoteric infor- *British Museum (Natural History), London.

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management 15-20 November 1961, Patancheru, A.P., India 3 mation in regard to them are unable definitely (America and Columbia [sic] are named on the title to interpret them without reference to later page) had sent him specimens of a large number of literature. If published with more definite data a new species, which he proposed to figure and at later dates, these names have their status describe in a work entitled Z u t r a g e zur Sammlung in regard to availability as of their date of exotischer Schmetterlinge. He then listed 75 com• such republication. binations of g e n e r i c plus specific n a m e s , a n d above each placed two numbers that ran consecu• By present-day standards, the combinations of tively from 1 to 150. Figure numbers 81 and 82 were generic plus specific name referred to in this sum• n a m e d Heliothis jucunda, a North American spe• mary would not be regarded as nomina nuda, pro- cies in a different subfamily from the European vided that the specific name was available within dipsacea. the meaning of the International Code of Zoological During the period 1808-1818, Hubner published Nomenclature (ICZN 1964) (Articles 10-15). The the plates of the first volume of his Zutrage zur unsatisfactory wording of the summary of Opinion Sammlung exotischer Schmettlinge (sic). The work 97 resulted in some authors continuing to argue w a s i s s u e d as a series of plates c o n t a i n i n g c o n • that the names were not properly rejected. Such secutively numbered illustrations. Each species was the vehemence expressed in publications that was figured twice, but no name or word of text the case was reopened, and in a ruling by the occurred on any of the plates. The plate containing Commission (ICZN 1954) in Opinion 278, the Ten- Figures 81 -82 was published by 1813, and these tamen was placed on the Official Index of Rejected illustrations, together with the name Heliothis and Invalid Works in Zoological Nomenclature as jucunda proposed in the 1808 Erste Zutrage, w o u l d Work No.14. The only nominal species included by h a v e m a d e Heliothis Hubner, 1813, nomenclatu• Hubner in his Tentamen concept of Heliothis w a s rally available for a generic concept entirely differ• Phalaena dipsacea Linnaeus, 1767, from Europe. ent from that in the Tentamen. What Hubner did in T h e Tentamen is now nomenclaturally dead, but his Erste Zutrage, was to place New World species its continuing relevance lies in the fact that from the in Old World genera. However, within a few years, time of its distribution in 1806, authors have used Hubner had realized that the New World species many of the generic names proposed in it, all of mostly represented different generic concepts and which were monotypic and based on Palaearctic therefore required different generic names. species. When Opinion 97 was being discussed in Accordingly, when in 1818 he published the text 1926, it was accepted that the next published use and descriptions to the illustrations, he usually of t h e Tentamen generic n a m e s w o u l d m a k e t h e m retained the same specific name that he had used nomenclaturally available. In the case of Heliothis, in his Erste Zutrage, but he proposed many new this next usage was believed to be by Ochsenhei- generic names. Figures 81 -82 were then named mer (1808), who included dipsacea L i n n a e u s a n d Melipotis jucunda. armigera Hiibner among the 14 nominal species he In order to resolve the nomenclatural chaos placed in his concept of this genus. Heliothis t h e n caused by the rediscovery of the Erste Zutrage, an became firmly entrenched in the European litera• application to the Commission was submitted by ture based on dipsacea Linnaeus, 1767 (a junior Nye (1964), requesting that the Erste Zutrage be subjective synonym of Phalaena viriplaca Huf- rejected for the purposes of zoological nomencla• nagel, 1766) as a type-species by subsequent ture on the grounds that it was a printer's proof and designation by Samouelle (1819). not published within the meaning of the Code. The After the Commission's rejection of the Tenta• Commission (ICZN 1966) agreed and ruled "that men, Hemming (1935) stated that he had "recently the incomplete pamphlet of Jacob Hubner, dated received a photostat copy of a very important and 1808, entitled Erste Zutrage zur Sammlung exo• hitherto unnoticed pamphlet published by Jacob tischer Schmetterlinge, has not been published Hubner in 1808." This work by Hiibner consisted of within the meaning of Article 8 of the Code, and a title page and four sheets printed on both sides therefore that neither the generic nor the specific and entitled Erste Zutrage zur Sammlung exo- names used in that pamphlet are available for tischer Schmetterlinge. A facsimile of this rare nomenclatorial purposes." The Erste Zutrage w a s work, known only from three copies, is provided by placed on the Official Index of Rejected and Invalid Hemming (1937). In a short introduction, Hubner Works in Zoological Nomenclature as Work No.72. stated that lepidopterists in foreign countries Under the same ruling, the name Heliothis Hubner,

4 1808, w a s p l a c e d on t h e Official Index of R e j e c t e d ion, d e p e n d i n g on t h e user's t e n d e n c y to lump or to a n d Invalid G e n e r i c N a m e s i n Zoology a s N a m e split, it is better to h a v e a b r o a d - b a s e d g e n u s Helio- No. 1857. T h u s t h e k n o w n n o m e n c l a t u r a l obsta• this for the s a k e of field workers a n d to divide it into cles to t h e u s e of Heliothis O c h s e n h e i m e r , 1 8 1 6 , s u b g e n e r a s u c h as Helicoverpa for t h e c o n v e n - h a v e b e e n r e m o v e d . However, t w o m o r e n o m e n - ience of taxonomists. W h y not have t h e best of b o t h clatural p r o b l e m s have arisen that affect, not the worlds? n a m e Heliothis itself, but first, the spelling of t h e T h e spelling of t h e subfamily n a m e b a s e d on subfamily n a m e b a s e d u p o n it, a n d s e c o n d , t h e Heliothis as t y p e - g e n u s d e p e n d s on w h a t is c o n s i • spelling of t h e specific n a m e s with w h i c h it is dered to be its correct stem. Boisduval (1928) first c o m b i n e d . u s e d t h e n a m e Heliothidi for a tribe containing Heli• T h e r e are other g e n u s - g r o u p n a m e s in the Helio• othis. S i n c e t h e n a n d up to the present day t h e this c o m p l e x , but Chlorides in particular w a s c o m • subfamily n a m e e n d i n g -inae has been a d d e d t o m o n in the literature in t h e first third of this century. Helioth- by s o m e authors a n d to Heliothid- by o t h • Chloridea D u n c a n [ & W e s t w o o d ] , 1 8 4 1 , w a s ers. Steyskal (1971) pointed out that the n a m e Heli- established for a single s p e c i e s Phalaena rhexiae othis is an aorist passive participle of t h e G r e e k Smith, 1 7 9 7 , w h i c h is a junior subjective s y n o n y m verb helioo, a n d strict application of the Interna- of Noctua virescens Fabricius, 1777, a n d distrib• tional C o d e , Article 29(a), w o u l d require t h e use of uted in N o r t h A m e r i c a . H a m p s o n (1903), in his the stem Heliothent- in f o r m i n g the subfamily major work on Lepidoptera, ignored t h e previous name. This has never bee n followed. Steyskal designations of dipsacea as t h e t y p e - s p e c i e s of continued: Heliothis a n d b a s e d his u s a g e of the n a m e on a different s p e c i e s Phalaena cardui Hubner, 1790, H o w e v e r , if Article 11 (b) of the Rules, w h i c h w h i c h is correctly the t y p e - s p e c i e s of Melipotis states that zoological n a m e s 'must be either H u b n e r [ 1 8 2 3 ] . H a m p s o n t h e n u s e d Chloridea for Latin or Latinized', be interpreted strictly, we dipsacea a n d armigera, and this interpretation w a s m a y consider that the c o m p l e x G r e e k parti• followed by W a r r e n (1914) in the s t a n d a r d refer• cipial s y s t e m w a s not part of Latin, e x c e p t in e n c e work, Die Gross-Schmetterlinge der Erde. the c a s e of a few w o r d s used as n o u n s a n d T h e result w a s c o n f u s i o n for t h e next quarter of a not to be f o u n d in Latin dictionaries. We m a y century, until Heliothis o n c e again r e g a i n e d a d o m • then consider Heliothis as declinable in the inant p l a c e in t h e literature. w a y t h e great majority of Latin n o u n s e n d i n g M o r e recently, Helicoverpa H a r d w i c k ( H a r d w i c k in is are declined. If this is done, t h e s t e m 1965b) w a s established, h a v i n g Noctua armigera u s e d in f o r m i n g family-group n a m e s will be H u b n e r (1808) as its t y p e - s p e c i e s , but authors Helioth- a n d the subfamily n a m e c o n s e • h a v e b e e n reluctant to adopt its use. B o u r s i n quently Heliothinae. (1965) p l a c e d Helicoverpa as a s y n o n y m of Chlori• dea, as at that time B o u r s i n u s e d Heliothis in t h e T h e n a m e Heliothinae is certainly in g e n e r a l , Erste Zutrage sense. Hardwick (1970) reiterated t h o u g h not in universal, use. In any c a s e it is c u s • with r e a s o n s his opinion that Helicoverpa a n d t o m a r y i n the Lepidoptera to a v o i d t h e c l u m s y Heliothis w e r e generically distinct. T o d d (1978), in -ididae or -idinae termination; for e x a m p l e , Pyralis, his " C h e c k l i s t of S p e c i e s of Heliothis Ochsenhei• family Pyralidae (Opinion 450) a n d Pieris, family mer," stated that " H a r d w i c k ( 1 9 7 0 : 1 8 ) feels that if Pieridae (Opinion 500). A n application t o t h e C o m • t h e c o r n e a r w o r m g r o u p (Helicoverpa H a r d w i c k , mission by Steyskal (1972) to h a v e the n a m e P y r a • 1965) is i n c l u d e d in Heliothis, t h e s p e c i e s of Schi- lidae c h a n g e d to Pyralididae w a s r e f u s e d in nia Hubner, 1 8 1 8 , s h o u l d also be transferred to Opinion 1094. In order to resolve t h e c o n f u s i o n , Heliothis. T h a t premise does not hold if t h e c h a r a c - Nye (1980) referred t h e c a s e t o t h e C o m m i s s i o n ters o n w h i c h his classification w a s b a s e d are a n d r e q u e s t e d a ruling that t h e s t e m of t h e g e n e r i c given a different weight of significance. A c c o r d • n a m e Heliothis O c h s e n h e i m e r , is Heliothis. T h e ingly, Helicoverpa H a r d w i c k is t r e a t e d as a s y n • C o m m i s s i o n has not yet voted on this application. o n y m of Heliothis, a n d t h e s p e c i e s of Schinia h a v e Up to t h e beginning of t h e present century, t h e not b e e n i n c l u d e d in this list." c o r n e a r w o r m a n d t h e c o t t o n bollworm w e r e u s u • My o w n view as a m u s e u m taxonomist, but for• ally treated in both the O l d a n d t h e N e w W o r l d as merly an agricultural entomologist, is that as o n e s o m e w h a t variable species, generally k n o w n g e n e r i c boundaries a r e generally a matter of o p i n - as Heliothis armigera (Hubner). But Aurivillius

5 (1897) s h o w e d that Bombyx obsoleta Fabricius g e n e r i c n a m e ; if Heliothis is treated as masculine, (Fabricius 1793) w a s t h e senior n a m e for this pest, t h e n armigera (the feminine form of a Latin adjec• so Heliothis obsoleta (Fabricius) gradually c a m e tive meaning 'bearing arms') would become into general use, particularly in North America. armiger. It is fortunate for our c o l l e a g u e s in t h e N e w Heinrich (1939) then indicated that Bombyx W o r l d that t h e n a m e of their s p e c i e s zea is a n o u n obsoleta s h o u l d not be u s e d , as it w a s a duplicate and therefore does not have to be changed to the of an order n a m e Bombyx obsoleta Fabricius, masculine form zeus. Their literature remains unaf• 1 7 7 5 , u s e d for a totally different s p e c i e s of m o t h in f e c t e d a n d they will not incur the w r a t h of t h e king of a n o t h e r family. So, o n c e again armigera c a m e into the Olympian gods by linking his name with that of a m o r e g e n e r a l , but not exclusive, use. It w a s C o m • major pest! mon (1953) who showed that armigera w a s res• Once again confusion has returned to the name tricted to the Old World and that the species in the armigera; so, in order to resolve the issue not only New World was distinct and had already been de• for armigera but also for t h e n a m e s of about 30 s c r i b e d as Heliothis umbrosus Grote (Grote 1862). other s p e c i e s p l a c e d in Heliothis that w o u l d also Before there was time for umbrosus to be adopted have to be changed to the masculine form, Nye in the literature, Todd (1955) showed that the oldest (1980) has reviewed the case and requested the n a m e for t h e N e w W o r l d pest s p e c i e s w a s Pha- Commission to rule that the gender of the generic laena zea Boddie (Boddie 1850) and so, as Helio- n a m e Heliothis is feminine. The Commission has this zea (Boddie) the name gained almost not yet v o t e d on this application. immediate acceptance and has been used thou- Such is the simplified saga of the scientific s a n d s of t i m e s ever since. n a m e s for t w o of t h e major pest s p e c i e s of t h e T h e u s e of armigera for the Old World species w o rl d . W h e t h e r to use Helicoverpa to denote a h a s b e e n extremely stable, but H a r d w i c k (1965) in g e n u s or a s u b g e n u s will a l w a y s r e m a i n a decision his masterly monograph on the corn earworm com• for t a x o n o m i s t s a n d not for the International C o m • plex, c i t e d Noctua barbara Fabricius as the oldest mission on Zoological Nomenclature, but the cor• n a m e for t h e s p e c i e s , but he t r e a t e d it as a nomen rect s t e m of Heliothis, as d i s c u s s e d above, a n d its oblitum and at the same time (Hardwick 1965a) g e n d e r for t h e p u r p o s e s of n o m e n c l a t u r e are d e c i • requested the Commission to rule that barbara sions that m u s t be m a d e by t h e C o m m i s s i o n . My should be suppressed. This the Commission application to the Commission has been strongly supported by colleagues. If you also agree with its a g r e e d to do in Opinion 1120 (ICZN 1979) and proposals, p l e a s e p a s s a resolution of support at Noctua barbara Fabricius w a s a c c o r d i n g l y p l a c e d this workshop and send it to the Secretary of the on the Official Index of Rejected and Invalid Spe• Commission for publication. c i f i c N a m e s i n Z o o l o g y a s N a m e No. 1045. T h u s all threats to the stable use of armigera were over• c o m e until Steyskal (1971) pointed out that the Note on Referendum g e n d e r of Heliothis was masculine and would require a ruling by the Commission to fix it as femi• At the International Workshop on Heliothis M a n • nine. In an Editor's Note at the end of Steyskal's a g e m e n t , w h i c h brought together m a n y of t h e p a p e r it w a s s u g g e s t e d that t h e c a s e s h o u l d be world's most experienced and active Heliothis referred to the Commission for a ruling. This was scientists, the nomenclature of Heliothis w a s dis• not done, presumably because no one anticipated cussed. Following the presentation of I.W.B. Nye's that anyone would wish to upset the traditional p a p e r o n t h e past a n d present c o n f u s i o n o f n o m e n • f e m i n i n e treatment of t h e g e n e r i c n a m e . clature in this genus, the participants were asked to Recently, T o d d (1978) in his " C h e c k l i s t of s p e • choose one of the following alternatives: c i e s of Heliothis Ochsenheimer" stated without any further c o m m e n t that " T h e g e n e r i c n a m e , Heliothis, 1. I support the retention of the established is m a s c u l i n e in gender, but has usually b e e n nomenclature for H. armigera, H. peltigera, H. treated as feminine. In addition, names proposed in punctigera, etc. feminine genera have been transferred to Heliothis 2. I support the suggested change in nomencla• u n c h a n g e d . All n e c e s s a r y c h a n g e s t o m a s c u l i n e t u r e to H. armiger, H. peltiger, H. punctiger, etc. endings have been made in this paper. As under the International Code, Article 30, an adjectival O f t h e 4 1 replies t o this r e f e r e n d u m , 3 9 c h o s e t h e specific name must agree in gender with the f o r m e r a n d 2 t h e latter. T h u s , this w o r k s h o p , by a

6 large majority, recommends to the International HEMMING, F. 1937. Hubner 1. London: Royal Entomo• Commission on Zoological Nomenclature that the logical Society of London. 605 pp. well-established Heliothis spp names, including ICZN (International Commission on Zoological armigera, peltigera, a n d punctigera, should con• Nomenclature). 1926. Opinion 97. Did Hubner's Tenta- tinue to be used. men, 1806, create monotypic genera? Smithsonian Mis • cellaneous Collections 73(4):19-30.

ICZN (International Commission on Zoological References Nomenclature). 1954. Opinion 278. Addition to the "Official List of Generic Names in Zoology" of the n a m e s of ten genera of the suborder Rhopalocera of the or d e r AURIVILLIUS, C. 1897. Bemerkungen zu den von J. Lepidoptera (Class Insecta), species of which were c i t e d Chr. Fabricius aus Danischen Sammlungen beschrieb- in the undated leaflet commonly known as the "Tenta - enen Lepidopteren. Entomologisk Tidskrift 18:139-17 4 . men", prepared by Jacob Hiibner, which is believed t o BODDIE, J.W. 1850. Insect physiology. II. Southern Cul• have been distributed to correspondents in 1806, a leaflet tivator 8:132. rejected in "Opinion 97". Opinions and Declarations R e n • dered by the International Commission on Zoological BOISDUVAL, J.A. 1928. Europaeorum Lepidopterorum Nomenclature 6:137-177. Index Methodicus. Paris. 103 pp. ICZN (International Commission on Zoological BOURSIN, C. 1965. Errata et addenda a mon travail Nomenclature). 1964. P a g e 1 7 6 i n International Code of "Les Noctuidae Trifinae de France et de Belgique" pa r u Zoological Nomenclature, 2nd ed. London, UK: Intern a • dans ce meme Bulletin, 1964, No. 6, p.204. Bulletin M e n - tional Trust for Zoological Nomenclature. suel de la Societe Linneenne de Lyon 34:182-187. ICZN (International Commission on Zoological COMMON, I.F.B. 1953. The Australian species of Heli• Nomenclature). 1966. Opinion 789. Rejection of the othis (Lepidoptera:Noctuidae) and their pest status. Aus • pamphlet by J. Hiibner, 1808, entitled Erste Zutrag e z u r tralian Journal of Zoology 1:319-344. Sammlung exotischer Schmetterlinge. Bulletin of Zoo l o g • FABRICIUS, J.C. 1793. Entomologia Systematica 3(1). ical Nomenclature 23: 213-220. 487pp. Hafniae. ICZN (International Commission on Zoological FABRICIUS, J.C. 1794. Entomologia Systematica 3(2). Nomenclature). 1979. Opinion 1120. Noctua armigera 349pp. Hafniae. Hubner, [1808] (Lepidoptera) conserved. Bulletin of Z o o • logical Nomenclature 35: 221 -222. GROTE, A.R. 1862. Additions to the catalogue of U.S. Lepidoptera. Proceedings of the Entomological Socie t y o f NYE, I.W.B. 1964. Application for the rejection for Philadelphia 1:218-219. nomenclatorial purposes of the pamphlet by J. Hubne r HAMPSON, G.F. 1903. Catalogue of the Lepidoptera entitled Erste Zutrage zur Sammlung exotischer Schmet• Phalaenae in the British Museum 4. London: British terlinge printed in 1808. Bulletin of Zoological Nomencla• Museum. 689 pp. 125 figs. ture 21: 58-80.

HARDWICK, D.F. 1965a. Noctua barbara Fabricius, NYE, I.W.B. 1980. Heliothis Ochsenheimer, 1816 1794 (Insecta, Lepidoptera): proposed rejection as a (Insecta, Lepidoptera): proposal to designate gende r a n d nomen oblitum. Bulletin of Zoological Nomenclature stem. Bulletin of Zoological Nomenclature 37: 186-1 8 9 . 2 2 : 1 0 1 . OCHSENHEIMER, F. 1808. Die Schmetterlinge von HARDWICK, D.F. 1965b. The corn earworm complex. Europa 4. Leipzig. 226 pp. Memoirs of the Entomological Society of Canada 40: SAMOUELLE, G. 1819. The entomologist's useful com• 1-247. pendium. London. 496 pp. HARDWICK, D.F. 1970. A generic revision of the North STEYSKAL, G.C. 1971. On the grammar of the name American Heliothidinae (Lepidoptera: Noctuidae). Heliothis Ochsenheimer (Noctuidae). Journal of the Memoirs of the Entomological Society of Canada 73: Lepidopterists' Society 25: 264-266. 1-59, figs. 1-114.

HEINRICH, C. 1939. The proper scientific name for the STEYSKAL, G.C. 1972. Application for correction of com ear worm. Journal of Economic Entomology. 32: certain names on the Official List of Family-Group N a m e s 5 9 5 - 5 9 6 . in Zoology. Bulletin of Zoological Nomenclature 29: 2 6 - 2 7 .

HEMMING, F. 1935. A note on Jacob Hubner's Erste TODD, E.L. 1955. The distribution and nomenclature of Zutrage zur Sammlung exotischer Schmetterlinge of the corn earworm. Journal of Economic Entomology 48 : 1808. Stylops 4.38-48. 6 0 0 - 6 0 3 .

7 TODD, E.L. 1978. A checklist of species of Heliothis Ochsenheimer (Lepidoptera: Noctuidae). Proceedings of the Entomological Society of Washington 80:1 -14.

WARREN, W. 1914. In Die Gross-Schmetterlinge der Erde, ed. A. Seitz, Stuttgart. 511 pp. 75 plates.

8 Heliothis: a Global Problem

W. Reed and C.S. Pawar*

Abstract

The geographical distribution of the major pests, Heliothis armigera, H. zea, and H. virescens, and the crop losses caused by these are reviewed. Although it is generally considered that the destruction of natural enemies by pesticide use and changes in cropping patterns and management have promoted these insects to major pest status, there are areas where H. armi• gera is a serious pest, although traditional agriculture is still practiced, and no pesticides are used. The dangers of a further increase in losses to Heliothis spp by breeding more susceptible crops are described. There is a need tor a more imaginative and holistic approach to research directed towards the management of these pests.

The Pests and Their Distribution their attraction a n d edibility. T h e g e o g r a p h i c a l range of H. armigera extends f r o m t h e C a p e V e r d e Of t h e m a n y r e c o r d e d Heliothis spp ( T o d d 1978), Islands in the Atlantic, through Africa, Asia, and only a f e w are of major i m p o r t a n c e as c r o p pests. Australasia, to the South Pacific Islands, and from H o w e v e r , the p o l y p h a g o u s nature a n d w i d e g e o • G e r m a n y in the north to N e w Z e a l a n d in t h e south. graphical spread of some of these (Hardwick 1965) It causes most damage in the semi-arid tropics, merit their consideration at an international level. however, and so is of prime interest to ICRISAT. Here at the International Crops Research Insti• Until the middle of this century, this insect had tute for t h e S e m i - A r i d T r o p i c s (ICRISAT), w e are b e e n c o n s i d e r e d to be identical to t h e c o t t o n boll- mainly concerned with Heliothis armigera (Hb.), a w o r m or c o r n e a r w o r m of the USA, w h i c h is n o w species that has been recorded as damaging 60 k n o w n as Heliothis zea (Boddie), thus accounting cultivated plant species and at least 67 other plant for t h e c o m m o n n a m e , A m e r i c a n bollworm, that is species in 39 families across Africa, Asia, and Aus• still u s e d to describe H. armigera t h r o u g h m u c h of tralasia. It is likely that this recorded list of host the Old World. Subsequently, however, Common plants is only a fraction of t h e total n u m b e r of plants (1953) w o r k i n g in Australia a n d Forbes (1 9 54) in on which this insect can, and does, feed. A system• the USA, concluded that there were specific differ• atic study of the host range is long overdue, for this ences between these insects. It has been generally c o u l d give information c o n c e r n i n g t h e c h e m i c a l a c c e p t e d that t h e s e t w o species, w h i c h are v e ry and physical attributes of plants that determine similar in all a s p e c t s , b e t w e e n t h e m c i r c l e t h e earth, with H. zea across the Americas and H.

*Pulse Improvement Program, ICRISAT, Patancheru, A.P., India. armigera stretching a c r o s s all t h e other tropical

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India 9 and subtropical countries, with no geographic the association of the use of arsenical dusts and overlap. the increased attacks by this pest. He recorded that This tidy and simple distribution has not gone in 1942-43 a general recommendation to farmers unquestioned, however, and there have been many not to dust their cotton led to a sharp decline of this suggestions that there is subspecies differentia• pest, largely through the resultant increase of its tion, and even differences that merit the erection of natural enemies, particularly in an area with a wide species among what are now regarded populations range of host plants. of H. armigera across the wide geographical range. The spectacular rise to infamy of H. virescens in Here in India, Bhattacherjee and Gupta (1972) dis• North America is so well known that we need not tinguished two species from within the commonly devote much time to this. Heliothis virescens h a d a c c e p t e d H. armigera. They considered that col• been recorded as a pest of cotton in Louisiana in lections from different plant hosts showed consist• the mid-1930s (Folsom 1936), but it was the wide• ent differences in taxonomy that merited specific spread use of DDT and other chemical pesticides separation. Subsequently, Bhatnagar (ICRISAT from 1950 to 1970, primarily to control Anthonomis 1976) studied the range of the cited taxonomic grandis Boheman, the boll weevil on cotton, that characters of insects collected from those host f o r c e d H. virescens into prominence (Adkisson plants and concluded there was continuous varia• 1971). The elimination of its natural enemies and bility within populations and no consistent differ• the resistance of the pest to all available pesticides ences associated with the collections from the allowed it to cause so much destruction that it different hosts. However, we frequently encounter closed down cotton growing in very large areas and puzzling differences in apparent host-plant prefer• so caused enormous economic upheaval. The e n c e s of H. armigera across and between areas publicity given to these events induced a wide• and cannot rule out the existence of at least sub- spread realization that chemical insecticides could specific differences between populations. For not be relied upon to insulate farmers from insect example, in southern India, at Coimbatore, H. pests, gave a tremendous boost to integrated pest management, and so led Adkisson to comment that armigera seldom reaches pest status on cotton, H. virescens had become a beneficial insect! but many moths of this species are caught in light traps through the cotton season, and this insect is a In addition to the "big three" Heliothis spp, there major pest on the legumes and other crops in this are others of localized or of minor-crop importance. area. A few miles to the south and a few hundred Heliothis punctigera (Wallengren) is a pest of a miles to the north, H. armigera is a very damaging wide range of crops in Australia. Heliothis peltigera pest of cotton in most years. (Schiff) is widely distributed across Europe, Africa, We have much to learn from such puzzles, and Asia, causing some damage to cotton and through the discovery of the reasons why Heliothis safflower. Heliothis assulta (Guenee) is wide• is not a pest on some crops and in some areas. spread through Asia and Australasia, with a differ• Unfortunately, we concentrate all of our efforts on ent subspecies occurring in Africa (Hardwick crops and areas where Heliothis is a major problem 1965), and causes some damage to solanaceous and await a brave, farseeing research supervisor c r o p s . Heliothis viriplaca (Hfn.), which earlier fea• who will direct his staff and funding to do otherwise! tured in the literature as H. dipsacea, merits pest The third most important species is Heliothis status on several crops, including cotton and sev• virescens (F.), which burst into prominence as a eral legumes, from southwest Asia well into USSR. major pest on cotton in the Americas in the middle of this century. Its common names, tobacco budworm and tomato budworm, reflect the crops on Losses Caused by Heliothis Spp which it caused most concern in both North Amer• ica and the West Indies in the early part of this As with many other pests, there are few well- century. Although this species had been recorded researched estimates of losses caused by the Heli- on cotton in the Virgin Islands by Wilson (1923) it othis spp. It has been generally assumed that the did not merit concern on this crop until the 1930s, losses are greatest on cotton, for it is on this cr o p when it was recognized as having become a major that these pests have received most attention. On pest of cotton in some areas of South America, cotton and other crops, Heliothis s p p f o r m only a particularly in Peru (Wille 1940). Hambleton (1944) part, but often a major part, of the pest complex, a n d reviewed the pest status of this insect and noted so it is difficult to apportion the losses, even wh e r e

10 t h e total losses are k n o w n . L o s s e s to H. zea in t h e g a t e d to minor status by m e a s u r e s — i n c l u d i n g a U n i t e d States have b e e n estimated to r e a c h reduction in pesticide u s e — t h a t will allow the n a t u • "hundreds of millions of dollars," and the losses to ral control e l e m e n t s to d e c i m a t e t h e populations. H. virescens t h r o u g h the 1960s a n d into t h e 1 9 7 0 s This simplistic approach has undoubted merit in must have reached similar sums. The cost of s o m e c a s e s , particularly in relation to H. virescens, c h e m i c a l s u s e d on c o t t o n to s u p p r e s s Heliothis but certainly not in the c a s e of H. armigera in m a n y spp w e r e estimated by Ignoffo (1973) to be in of its endemic areas. excess of $50 million per year. Heliothis zea was a major pest of several crops, In Australia, Alcock and Twine (1980) estimated including maize a n d cotton, well before the w i d e • that Heliothis s p p cost over $ 1 6 million in t h e state spread use of pesticides. At the turn of the century it of Q u e e n s l a n d alone e a c h year, with major losses w a s c o n s i d e r e d to be of sufficient i m p o r t a n c e to on sorghum, cotton, tomatoes, tobacco, and saf- merit a 1 4 9 - p a g e U S D A Bulletin ( Q u a i n t a n c e a n d flower, a n d with substantial losses on 11 other Brues 1905), a n d H y s l o p (1927) c o n s i d e r e d this to crops. T h e s e estimates i n c l u d e d both the cost of be the third most destructive pest in t h e USA. protection d e s i g n e d to r e d u c e c r o p loss a n d t h e Heliothis armigera has bee n the d o m i n a n t a n d residual losses. Elsewhere in Australia, the des• primary pest of cotton in some countries of Africa, truction of natural enemies and resistance of Helio- including Tanzania, both before a n d after pesti• this spp to insecticides (Wilson 1974) led to a cides became widely used. In India it is the domi• situation i n the O r d s c h e m e w h e r e t h e pests c o u l d nant pest on cotton in s o m e areas a n d on s e v e r a l no longer be controlled, a n d c o t t o n - g r o w i n g h a d to other crops, particularly pigeonpea and chickpea, b e d i s c o n t i n u e d , s o leading t o large l o s s e s a n d t h e in m o s t areas. On b o t h t h e major pulse c r o p s , H. need for a substitute crop that was not susceptible armigera commonly destroys more than half the to Heliothis a n d c o u l d be g r o w n profitably. In Africa, yield, yet e v e n n o w less t h a n 1 0 % of the f a r m e r s t h e r e appear to be no recent estimates of losses in use any pesticides on t h e s e or other c r o p s on cash terms. It is not difficult to estimate, however, which this pest is particularly damaging. In such that t h e loss of cotton to H. armigera in T a n z a n i a circumstances, the pest status cannot be attrib• alone must a m o u n t to m o r e t h a n $ 2 0 million in most uted to man's m i s u s e of pesticides a n d t h e a n s w e r years, a loss that may appear s m a l l in t h e d e v e • is certainly not a reduction of pesticide use. loped countries, but is a massive sum when related It is commonly considered that Heliothis s p p a r e to the economy of that developing nation. In Sudan, b e c o m i n g an increasing problem, this being a s s o • this pest is n o w c o s t i ng t h e Gezira a n d other c o t t o n ciated with improving agriculture. Quantitative evi• schemes enormous sums both in yield losses and d e n c e of increasing intensity or e x t e n s i o n of t h e in pesticide costs. areas of attack is available from only a few areas, In India, there are no published estimates of however, for there are usually no b a s e data of losses c a u s e d by H. armigera, but calculations quantitative records of populations or losses. based upon ICRISAT surveys of farmers' fields T h e r e is little doubt that Heliothis s p p i n c r e a s e d indicate that t h e annual loss of t h e t w o major in i m p o r t a n c e in t h e U n i t e d States largely b e c a u s e pulses, chickpea and pigeonpea, may exceed of pesticide use, but partly also because of a gen• $300 million per year, and losses in other legumes, eral i mp ro v e me n t in cropping, leading to higher cotton, cereals, and other crops must add substan• yields through the use of inputs such as fertilizer tially to that total. Such estimates certainly justify a n d irrigation. We know that H. armigera h a s the i n c r e a s e d r e s e a r c h attention that is n o w being i n c r e a s e d in i m p o r t a n c e in S u d a n a n d Egypt, paid to this pest. apparently for similar reasons. In northern Nigeria, H. armigera w a s a rarity in the late 1 9 5 0 s , but h a s since become a pest; this increase was perhaps What Promotes Heliothis Spp to associated with t h e introduction of m a i z e a n d Pest Status? t o m a t o e s in irrigated s c h e m e s . In India, t h e pest populations are at present greatly reduced each

T h e H. virescens s a g a in t h e U S A c o n v i n c e d s o m e year by the hot dry s u m m e r s in t h e s o u t h a n d t h e c o l d winters i n t h e north. W e fear that a n i n c r e a s e i n scientists that the pest status of Heliothis s p p has t h e u s e of irrigation in the s o u t h is leading to an been almost entirely pesticide-induced. Conse• increase in the availability of plant hosts through quently all Heliothis s p p h a v e recently b e e n t h e dry s e a s o n a n d a s u b s e q u e n t i n c r e a s e in pest regarded as "upset pests" that can be easily rele-

11 populations. We also suspect that there are sub• ing the incidence and extent of moth migration. stantial long-range migrations of the moths, so the Disruption of the natural control elements of H. north may face increasing populations as a result armigera can also occur during migrations from of developments in the south. area to area and during shifts from one host to Scientists in the USA have demonstrated that the another in the same area. This latter effect has factors regulating populations of H. zea are fairly been clearly shown (Bhatnagar et al.: these Pro- well understood, for computer programs combining ceedings) in the case of sorghum and pigeonpea, these factors now permit the forecasting of popula• for on these crops the pest transfers from one to the tions across areas with reasonable accuracy other, but many of the natural enemies do not. (Hartstack et al. 1976). For H. armigera, however, Although most blame for increases in Heliothis our knowledge of what promotes differing popula• problems has been attributed to the destruction of tions across areas and years is woefully natural control by pesticides, there is some evi• inadequate. dence that plant breeders have also contributed. Perhaps the most important observation towards Progress in breeding for resistance to Heliothis in understanding H. armigera populations was made the major host crops has been slow, and there are by Coaker (1959), while working in southern few instances of new cultivars particularly selecte d Uganda. He noted that H. armigera was not a for their resistance or tolerance to Heliothis being serious pest of cotton in that area, but within 200 released to farmers. Most breeding and subse• miles, both to the north in Uganda and to the south quent testing of Heliothis-susceptible crops, partic• in Tanzania, this pest was severe on cotton. He ularly in the developing countries, are carried out in concluded that in southern Uganda, the insect did pesticide-protected fields, with yield as the main not achieve pest status because the climate selection criterion. We have some evidence from allowed both the insect and its natural enemies to trials at ICRISAT that such selection is likely to lead thrive throughout the year. In northern Uganda and to increased losses to Heliothis and other pests. in Tanzania, however, there are prolonged dry sea• Good examples of this are (1) the determinate type sons during which few host plants provide food for pigeonpeas, which can yield well under pesticide the insects, so populations of the pest and its nat u • protection but yield virtually nothing in unprotect e d ral enemies are reduced to very low levels each fields in southern India, and (2) the tight-head sorghums, which do well under protected condi• year. In the rainy season, H. armigera population tions but are much more severely attacked by Heli• increases outpace those of its natural enemies. By othis and other pests than the open-head types of the time the natural enemy populations build up to sorghum in farmers' fields (Doggett 1954). Here at influential levels, the damage to crops has already ICRISAT we appear to be unique among research b e e n d o n e . stations in retaining large areas of land that are Given such evidence, we may be totally wrong in pesticide-free, and these are being increasingly fearing that an increase in the availability of hosts utilized not only by the entomologists but also by through the dry season may give India increasing our breeders and other scientists. Heliothis spp problems. Here at ICRISAT we insist upon a closed season during which no crops may be grown, in an attempt to control some pests, including Atherigona soccata, the sorghum shoot The Future fly. There is at least a possibility that such clos e d seasons could lead to an increase in H. armigera In the past, a great deal of research effort was populations as a result of a reduction of the natural expended upon Heliothis spp, but usually on single enemies. We may be providing a disruption of the crops, particularly cotton, and within small areas, natural control and so promoting the pest, just as sometimes within research station boundaries. pesticide use has done. We now have to consider Much of the research has been directed towards whether we can find evidence that will determine single elements of pest management and the litera• whether a closed season is beneficial or harmful to ture is rich in such information. In spite of all this the pest status of H. armigera in any area. It is work, however, we have little to offer farmers in t h e unlikely that we will be able to contrive a replicated semi-arid tropics of the developing countries in th e experiment that will allow us to test this in our fields, way of practical reduction of Heliothis-caused so we may have to rely upon computer simulations, losses on their crops, other than to advise them to if we can determine the meaningful inputs, includ• use one or two pesticide applications. We are

1 2 nowhere near a situation where we can provide BHATNAGAR, V.S., LATEEF, S.S., PAWAR, C.S., practical integrated pest management on a SITHANANTHAM, S., and REED, W. 1982. R e s e a r c h national, area, or even field basis, that can compe t e on Heliothis at ICRISAT. These Proceedings. with the immediate economic advantage of using DDT BHATTACHERJEE, N.S., and GUPTA, S.L. 1972. A new species of Heliothis Ochsenheimer (Noctuidae, Our failure may be a result of the restriction of Lepidoptera) infesting cotton and tur (Cajanus indicus) in most research to individual crops or fields. We India with observations on the three other common s p e • need a more holistic approach, with emphasis cies of the genus. Journal of Natural History 6:147 - 1 5 1 . u p o n Heliothis populations over areas and over time. ICRISAT is ideally placed to encourage such COAKER, T.H. 1959. Investigations on Heliothis armig- research across India and has already embarked era (Hb.) in Uganda. Bulletin of Entomological Rese a r c h upon this in cooperation with scientists of the 50: 481 -506. Indian Council for Agricultural Research and those working in other national and state institutes. In COMMON, I.F.B. 1953. The Australian species of Helio- Australia, there is a team in Queensland that has this (Lepidoptera: Noctuidae) and their pest status. Au s - been concentrating upon Heliothis management tralian Journal of Zoology 1: 319-344. and their work may well act as a model for other areas. In Africa, there appears to be no well-funde d DOGGETT, H. 1954. I n Progress Report for the season or multidisciplinary team effort to fight Heliothis, 1952-53, Tanganyika Territory, Lake Province. Empir e except in the Sudan. In the United States there Cotton Growing Corporation. London U.K. have been some magnificent individual contribu• tions to the understanding and management of FOLSOM, J.W. 1936. Notes on little known cotton Heliothis spp, but even there greater progress insects. Journal of Economic Entomology 29(2): 282- 2 8 5 . could have been made if there had been integration FORBES, W.T.M. 1954. Lepidoptera of New York and of effort on an area, rather than on a crop, basis. neighbouring states. III. Noctuidae. Cornell Agricu l t u r a l We hope that this workshop will promote not only Experiment Station Bulletin 329, Ithaca, NY, USA. 4 3 3 p p . the interchange of information and ideas between scientists working on different aspects, on different HAMBLETON, E.J. 1944. Heliothis virescens as a pest crops, and in different countries, but will also st i m u • of cotton, with notes on host plants in Peru. Journ a l of late a reappraisal of research policies that will Economic Entomology 37(5): 660-666. result in more coordination of individual and local • ized research. If such a reappraisal is not made, HARDWICK, D.F. 1965. The corn earworm complex. there is a danger that there will be another work• Memoirs of the Entomological Society of Canada 40, shop 80 years in the future, discussing similar pro b • Ottawa, Canada. 247 pp. lems and prospects. Those who have studied Quaintance and Brues' (1905) report will realize HARTSTACK, A.W., WITZ, J.A., HOLLINGSWORTH, J.P., RIDGWAY, R.L., and LOPEZ, J.D. that much of the Heliothis research today is doing 1976. MOTHZV-2: A computer simulation of Heliothis little more than rediscovering what was reported at zea a n d Heliothis virescens population dynamics. Users the beginning of this century! manual. U.S. Department of Agriculture ARS-S-127, Washington DC, USA.

References HYSLOP, J.A. 1927. A monthly survey report. Journal of Economic Entomology 20: 717-725.

ADKISSON, P.L. 1971. Objective use of insecticides in ICRISAT. 1976. Pages 178-180 i n ICRISAT Annual agriculture. Pages 43-51 i n Proceedings, Symposium on report 1975-76. Patancheru, A.P., India: ICRISAT. Agricultural Chemicals—Harmony or Discord for Food, People and the Environment (ed. J.E. Swift). Univer s i t y o f California, USA. IGNOFFO, C.M. 1973. Development of viral insecticide concept to commercialisation. Experimental Parasito l o g y ALCOCK, B., and TWINE, P.H. 1980. The cost of H e l i o - 33: 380-406. this in Queensland crops. Presented at the Workshop on Biological Control of Heliothis spp. 23-25 Sept 1980, QUAINTANCE, A.L., and BRUES, C.T. 1905. T h e c o t - Queensland Department of Primary Industries, Too- ton bollworm. U.S. Department of Agriculture. Burea u o f woomba, Queensland, Australia. Entomology, Bulletin 50, Washington, DC, USA. 149 p p .

13 TODD, E.L. 1978. A checklist of species of Heliothis Ochsenheimer (Lepidoptera: Noctuidae). Proceedings of the Entomological Society of Washington 80(1):1 -14.

WILLE, J.E. 1940. Observations sobre Heliothis virescens F. como plaga del algodonero en el Peru (Lep). Revista de Entomologia (Rio de Janeiro) 11(1-2): 584- 588.

WILSON, A.G.L. 1974. Resistance of Heliothis armigera to insecticides in the Ord Irrigation Area, North Western Australia. Journal of Economic Entomology 67:256-258.

WILSON, C.E. 1923. Insect pests of cotton in St. Croix and means of combatting them. Virgin Isles Agricultural Experiment Station Bulletin 3, Virgin Isles.

14 Session 1

Biology, Behavior, and Ecology of Heliothis Spp

Chairman: E.G. King Rapporteurs: S.S. Lateef Cochairman: R.C. Patel S. Sithanantham

Biological and Ecological Studies of Heliothis

S. Jayaraj*

Abstract

The previous work on the biology and ecology of Heliothis spp is reviewed and recent work in South India is reported. Heliothis armigera laid 50.6% eggs on the upper surface of cotton leaves on the upper half of the plant. Squares were the other preferred site, with a mean of 31.7% eggs. Temperature and host plant affected the development of H e l i o t h i s considerably. The preferred host plants for oviposition by H. armigera were found to be, in descending order, pigeonpea, field bean, chickpea, tomato, cotton, chillies, mung bean, and sorghum. Feeding preference was, in descending order, pigeonpea, field bean, cotton, sunflower, sorghum, chickpea, mung bean, urd bean, and tomato. Chillies were not selected tor feeding. A mean of 76.9 larvae per three plants was observed on pigeonpea grown as a border crop around cotton, but a mean of only 4-05 larvae was found on the main cotton crop. Consumption index (fresh weight) had significant correlation with innate capacity for increase in numbers and finite rate of increase; growth rate was significantly correlated with the net reproductive rate, weight of pupae, and percentage of pupae and moths formed.

Heliothis spp are major pests on many important spp because of their wide distribution in many parts crops, H. zea (Boddie), H. armigera (Hiibner), and of the world; the literature pertaining to the biology H. virescens (F.) being the most devastative. In and ecology of the important species is briefly India, the three species—H . armigera, H. peltigera reviewed in this paper. Schiff, and H. assulta Guenee—occur frequently, a n d H. armigera is by far the most important. A great deal of information is available on Heliothis Annual Cycle

Heliothis armigera passes through four genera- *Tamil Nadu Agricultural University, Coimbatore, India. tions in the Punjab, India: one on chickpea during

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. 17 March; two on tomato, from the end of March to was extremely important from an economic stand• May; and one on maize and tomato in July-August point. The final generation in late September and (Singh and Singh 1975). Light-trap catches also early October was also found on these plants. showed the occurrence of four broods. Moths of Cotton was infested in mid-July, and infestations the first brood appeared in March; of the second in were more or less continuous until the crop was April; of the third in May; and of the fourth in July- removed in September-October. Soybeans often August. Bhatnagar (1980) reported that seven to supported heavy populations in late August and eight generations of H. armigera are present each early September. Diapause populations developed year in Andhra Pradesh, India. in October, mostly on regrowth cotton. Oviposition usually starts in early June, with the Like the bollworm, the tobacco budworm, H. onset of premonsoon showers, adults possibly virescens, is found on a variety of weed hosts and emerging from diapausing pupae and also from legumes in the first generation. Tobacco is the larvae that had been carried over in low numbers favored host for the second and later generations, on crops and weeds during the summer. Repro• but in the absence of tobacco, cotton is the princi• ductive moths were recorded throughout the year pal summer host. Tomato, okra, and alfalfa may be ovipositing on the host crops and weeds with flow• locally important, but corn and grain sorghum are ers. The pest multiplied on weeds, early-sown corn, seldom infested (Lincoln 1972). sorghum, mung bean, and groundnut before infest• Generalizations about seasonal abundance ing pigeonpea in October-November and chickpea must, however, be limited to areas with similar cli• in November-March. Field surveys have indicated mate, crops, and wild hosts. that the larvae of H. armigera axe present on some crop or weed host in every month of the year. Host plants flowering in summer and weed hosts are a Life History and Habits source of carryover. Hsu et al. (1960) observed three generations of H. armigera each year in Moth Activity China. The pest bred four complete and a partial fifth generation in Hunan Province of China (Ano• Details of the life history and habits given for H. nymous 1977). Reed (1965) reported that the pest armigera appear to be broadly similar to those completed four generations from September to g i v e n for H. zea (Pearson and Darling 1958). March under western Tanganyika conditions. Although emergence of H, armigera m o t h s has The literature on seasonal abundance of H. zea been found to take place in the evening any time a n d H. virescens has been reviewed by Lincoln after 1600 hr, the peak emergence being between (1972). Development of the bollworm, H. zea, has 2000 and 2200 hr (Singh and Singh 1975; Roome been found to be continuous, at least at a low level, 1975). There was no emergence during the day. throughout most years in southern Louisiana Roome (1975) observed that from 0200 to 0400 hr (Brazzel et al. 1953) and in the lower Rio Grande the males flew above the crop while the females Valley (Fife and Graham 1966). At more northerly were stationary and released a pheromone. During locations, Heliothis survived the winter as diapaus• this period of high male and low female activity, ing pupae in the soil and there were then six gener• assembly of males around females and copulation ations in the year. The first generation in the spring were observed in caged as well as field conditions. was found on a variety of weed and legume hosts; Inseminated female H. armigera were collected in larvae were generally exposed to parasites and crops that were at a suitable stage for oviposition, predators, because the fruiting bodies of the hosts while light traps away from crops or near mature were too small for larvae to bore into. The second crops collected mainly virgin females. Loganathan generation in early and mid-June was passed prim• (1981) observed peak mating activity at 0400 hr. arily on whorl-stage corn, tomato, tobacco, alfalfa, The preoviposition period ranged from 1 to 4 okra, and cotton. Two generations were passed on days, oviposition period 2 to 5 days, and p o s t p o - corn, which silks continuously from mid-June to sition period 1 to 2 days (Patel et al. 1968; Singh a n d late July, depending on the planting date. From Singh 1975). Moths continued to oviposit for 10 to early August, with the loss of corn as a suitable 23 days in South Africa, depending on the time of host, the fifth generation turned to a series of hosts, year, averaging 730 eggs each, with a maximum of and cotton, groundnut, alfalfa, and tobacco were all 1600, and a maximum in one night of 480. In South- found to support large populations. This generation ern Rhodesia, the total number of eggs laid over a

18 period of 2 m o n t h s r a n g e d up to 1729, a n d t h e approximately one-third of the d i s t a n c e in n o d e s a v e r a g e per egg-laying night up to 2 7 6 . In the USA, from the terminal. The main-stem leaves were the o n e m o t h laid a m a x i m u m of about 3 0 0 0 eggs. preferred oviposition sites. Older larvae w e r e f o u n d Oviposition on maize by H. zea mostly took place at lower on the plant than y o u n g e r ones, a n d early the t i m e of silking, but by H. armigera at the time the first-instar larvae were detected in squares by the tassels appear. On cotton, oviposition rarely took presence of trass and flaring of the bracts. p l a c e in quantity until flower buds w e r e f o r m e d Patel et al. (1974), found that, irrespective of the (vide P e a r s o n a n d Darling 1958). color (yellowish green or deep-green) of the cotton plants, H. armigera preferred t h e upper half of t h e plant to t h e lower, the upper leaf s u r f a c e s to t h e Eggs lower, a n d tender leaves to m e d i u m a n d old leaves for oviposition. In the yellowish green fields, m o r e T h e eggs of Heliothis armigera are nearly s p h e r i • eggs w e r e laid on the o c c a s i o n a l d e e p g r e e n plants cal, with a flattened base, giving a s o m e w h a t t h a n on yellowish ones, but n u m b e r of e g g s per 50 dome-shaped appearance, the apical area sur• leaves w a s still greater in the wholly d e e p g r e e n rounding the micropyle smooth, the rest of the sur• fields, indicating that ovipositing females were f a c e s c u l p t u r e d in the form of longitudinal ribs; at attracted to d e e p green. first yellow-white, glistening, changing to dark T h e incubation period of the eggs is longer in b r o w n before hatching; diameter 0.4 to 0.55 m m . cold w e a t h e r a n d shorter in hot weather, being 2 to T h e e g g s are laid singly, late in t h e evening, 8 days in South Africa a n d 2.5 to 17 in t h e United mostly f r o m after 2 1 0 0 hr to midnight. On m a n y host States (Pearson a n d Darling 1958), a n d 2 to 5 d a y s plants, t h e e g g s are laid o n t h e lower s u r f a c e o f t h e in India (Srivastava a n d S a x e n a 1958; S i n g h a n d leaves along t h e midrib. Eggs are also laid on t h e Singh 1975) a n d W e s t e r n T a n g a n y i k a (Reed 1965). buds, flowers, a n d in b e t w e e n t h e calyx a n d fruit The viability of eggs varies from 63 to 90%. ( C o n t i n h o 1965; Singh a n d Singh 1975). H. zea in t h e U n i t e d States, w h e n laying e g g s on maize, pre• fers the silks, but H. armigera in South Africa lays Larvae very few eggs on the silks a n d about half on t h e stalks. On cotton, H. armigera e g g s w e r e f o u n d There are normally six instars in H. armigera, but mostly on the upper s u r f a c e s of leaves a n d on t h e exceptionally, during the cold s e a s o n , w h e n larval squares, while H. zea laid one-third on t h e squares development is prolonged, seven instars were reg• a n d the remainder s c a t t e r e d about the plant (vide ularly f o u n d in Southern Rhodesia (Pearson a n d Pearson a n d Darling 1958). Darling 1958). T h e newly h a t c h e d larva is translu• B e e d e n (1974) o b s e r v e d that e g g s of H. armig• cent and yellowish white in color, with faint yellow• era were laid on cotton uniformly over the field ish o r a n g e longitudinal lines. T h e h e a d , t h o r a c i c throughout the season. A significant correlation a n d anal shields, a n d legs are b r o w n , a n d t h e s e t a e w a s f o u n d b e t w e e n the n u m b e r of s y m p o d i a l dark brown (Neunzig 1964; Singh a n d S i n g h 1975). n o d e s a n d t h e n u m b e r of e g g s per plant throughout T h e full-grown larva is about 35 to 42 mm long; the s e a s o n . T h e f a v o r e d oviposition sites c h a n g e d general body color is pale g r e e n , with o n e b r o k e n from vegetative parts of plants, notably leaf surfa• stripe along e a c h side of the body a n d o n e line on c e s a n d s t e m s , early in the s e a s o n to bolls a n d the dorsal side. Short white hairs are s c a t t e r e d all over the body. H e a d is reddish b r o w n , t h o r a c i c a n d p e d u n c l e s later in the s e a s o n . anal shields a n d legs are b ro w n. Setae are dark, T h e p e r c e n t a g e of oviposition by H. armigera on prothorax is slightly m o r e b ro w n i sh t h a n m e s o - a n d cotton w a s f o u n d to vary on t h e s u r f a c e s of leaves meta-thorax. Crochets are arranged in a biordinal in t h e upper a n d lower halves of the plant in the symmetry on the prolegs. The underside of the early, peak, a n d late flowering phases. A m e a n of larva is uniformly pale. The general color is 5 0 . 6 % e g g s w a s o b s e r v e d o n t h e upper s u r f a c e o f extremely variable; a n d t h e pattern m a y be in leaves on the upper half of t h e plant. C o t t o n shades of green, straw yellow, and pinkish to red• s q u a r e s f o r m e d t h e other preferred site, with a dish b r o w n or e v e n black. m e a n of 3 1 . 7 % e g g s ( T a b l e 1). T h e lower s u r f a c e of leaves on the lower half of the plant was the least T h e y o u n g larva of H. armigera on e m e r g i n g preferred site (Vijayakumar a n d J a y a r a j 1981). A usually eats some or all of its empty eggshell before study of within-plant distribution of H. zea on cotton feeding on the plant. It wanders about nibbling var• revealed that t h e a v e r a g e location of eggs w a s ious parts of the plant until it finds a flowerbud or

19 Table 1. Oviposition pattern of H . armigera on cotton during early, peak, and late flowe r i n g p h a s e s ( m e a n o f three observations).

Percentage eggs laid during

E a r l y P e a k L a t e f l o w e r i n g f l o w e r i n g f l o w e r i n g ( A u g u s t - ( O c t o b e r - ( D e c e m b e r ) Place of oviposition S e p t e m b e r ) N o v e m b e r ) M e a n

S q u a r e s 2 8 . 4 3 3 . 3 3 3 . 4 3 1 . 7 ( 3 2 . 3 ) ( 3 5 . 4 ) ( 3 5 . 3 ) ( 3 4 . 3 )

Leaves: Upper half of plant Upper surface of leaf 4 5 . 9 5 3 . 7 5 2 . 1 5 0 . 6 ( 4 2 . 0 ) ( 4 7 . 2 ) ( 4 6 . 3 ) ( 4 5 . 2 ) Lower surface of leaf 1 7 . 2 9 . 3 1 4 . 6 1 3 . 7 ( 2 4 . 6 ) ( 1 7 . 8 ) ( 2 2 . 2 ) ( 2 1 . 5 )

Leaves: Lower half of plant Upper surface of leaf 7 . 7 3 . 6 0 . 0 3 . 8 ( 1 6 . 1 ) ( 1 0 . 7 ) ( 1 . 8 ) ( 9 . 5 ) Lower surface of leaf 0 . 8 0 . 0 0 . 0 0 . 3 ( 4 . 2 ) ( 1 . 8 ) ( 1 . 8 ) ( 2 . 6 )

L S D ( P = 0 . 0 5 )

Stage of flowering 1 . 6 2 * * ( F i g u r e s i n p a r e n t h e s e s a r e P l a c e 2 . 0 8 * * arcsin percentage values) Stage of flowering x 3 . 6 0 * * p l a c e ** Significant at 1% level

Source: Vijaykumar and Jayaraj (1981).

flower; a b u d will be hollowed out, leaving an e m p t y (Wilcox et al. 1956), a n d 8 to 12 days in the Punjab, shell. Young larvae rarely attack bolls; older larvae India (Singh a n d Singh 1975) on the s a m e host, prefer b u d s a n d y o u n g bolls. T h e full-grown larva is tomato. T h e length of larval life is r e c o r d e d as 15 to of considerable size and it habitually feeds with 32 days in South Africa, 14 to 70 in t h e United only t h e front portion of its body inside t h e hole it States, a n d 18 to 35 in N y a s a l a n d . In Southern has made. Cotton buds and bolls that have been Rhodesia, the larval period a n d the t e m p e r a t u r e in a t t a c k e d by Heliothis thus commonly show an an insectary averaged approximately 18 days accumulation of larval faeces between the surface (22.5°C) in N o v e m b e r a n d 51 d a y s (17.5°) in J u n e - and the enclosing bracteoles. This habit must July. T h e t e m p e r a t u r e limits d e t e r m i n e d in the render the larva m o r e p r o n e to attack by natural USSR w e r e 14 a n d 36°C; the o p t i m u m temperature, enemies. T h e larvae often m o v e about the plant 27 to 28°C at 1 0 0 % relative humidity for the early and usually attack each other if they meet; the instars a n d 25 to 26°C at 80 to 9 0 % for the late victor, if not mortally wounded, will devour its instars (vide Pearson a n d Darling 1958). opponent. Nikishina (1980) reported that temperature also Temperature affects the development of the regulates feeding activities of H. armigera larvae larva considerably. T h e larval duration varied f r o m that give rise to overwintering p u p a e in Tadzhikis- 21 to 40 d a y s in California, 18 to 51 d a y s in O h i o tan, USSR. T h e larvae f e d on fruiting forms, irres-

2 0 pective of the amount present of the sex hormone hand lens, whether a pupa is in diapause or not. vitamin E (tocopherol), but the proportions of pupa e The fat body of the newly formed pupa is composed entering diapause varied with the forms on which of firm, rounded lobes, and remains unchanged in the larvae fed. Third-generation larvae in fields of this condition throughout diapause. In the develop• early cotton fed mainly on squares and 10-day-old ing pupa, histolysis starts on the second day and bolls containing in all 74.7 mg of vitamin E/100g the fat body disintegrates into a mass of minute, and later on buds and squares containing 47.5 free granules; these start to re-form, about half-way mg /100g. Diapausing pupae in the two cases were through the life of the developing pupa, into the 18.5% and 24.5% respectively. adult fat body, which is in the form of digitate lobes The rate of development of H. armigera is also lying along the trachea (vide Pearson and Darling affected by the type of food. The larval stage lasted 1958). for 21 to 28 days on chickpea (Srivastava and The nondiapause pupal period for H. armigera Saxena 1958); 21.8 days on maize silk; 33.6 days was recorded as 14 to 40 days in the Sudan Gezira, on sunflower corolla (Coaker 1959); and 20 to 21 14 to 57 in Southern Rhodesia, 12 to 25 in Tanga• days on cotton (Hsu et al. 1960; Reed 1965). nyika, 14 to 37 in Uganda, 15 to 25 in Nyasaland, The full-grown H. armigera larva leaves the plant, and 5 to 8 days in India; for H. zea, this period was sometimes by dropping to the ground, and burrows recorded as 14 to 40 days in the United States. into the soil to a depth of 2.5 to 17.5 cm. In the c a s e Experiments conducted at controlled temperatures of H. zea, the larva then works upward by a different in the United States gave 10.3 days as the pupal route, forming a curved tunnel with smooth walls of period of H. zea at 32°C and 26.7 days at 20°C. well-packed earth, thinly covered with silk. This Experiments in the USSR, in which the pupal stage burrow stops just below the surface, and the larva of H. armigera took from 13 days at 25°C to 36.6 then retires to the lower end where it pupates (vide days at 17.1°C, suggested 11°C as the threshold of Pearson and Darling 1958). In sandy soil the bur• development, although larvae bred at 27 to 28°C row is deeper when the soil is dry; in heavy soil it is produced only a few moths, some of them shallow, and if the soil is very dry, the larva may not deformed, when the pupae were kept at 14 to 15°C. be able to penetrate it and uses a crack instead. The date of emergence of adults from diapause pupae in southern Africa is more or less independ• Pupae ent of the date of formation of the pupae, those formed in March to June contributing impartially to The pupa is 14 to 18 mm long, mahogany-brown, an emergence broadly covering August to mid- smooth-surfaced, and rounded both anteriorly and October. According to Pearson and Darling (1958), posteriorly, with two tapering parallel spines at the this suggests that diapause development is posterior tip. accomplished in two parts, with different tempera• Harrell et al. (1979) studied the effects of two ture requirements, the first having a relatively low levels of temperature (25 and 29°C), two of relative requirement, so that all diapause pupae complete it humidity (50 and 70%), and five of air velocity (10, during the winter months and are then arrested, 75,150, 200, and 300 cm/sec) on development of pending the onset of higher temperatures that ena• H. zea. Relative humidity influenced the develop• ble the second part to be accomplished by all ment more than air velocity. The higher tempera• pupae more or less concurrently, the later formed ture shortened pupation time. Air velocities did not ones having by then caught up with those formed affect development at high humidity but did at low earlier. humidity. Diapause in H. armigera is most pronounced in The pupa of H. armigera undergoes a facultative South Africa and Southern Rhodesia. It also occurs diapause. Only nondiapause pupae are formed in the Eastern Province of what was formerly Tan• during much of the year, but during cold weather, a ganyika, but is not as pronounced as further south, large proportion of the pupae formed undergo dia• and in Uganda, on the Equator, no definite dia• pause and thus have a considerably extended pause occurs. In the Sudan Gezira, a succession of pupal period. Not all pupae, however, enter dia• short-term generations occurs between August pause, even in the coldest months, although the and January, and in each generation an increasing duration of the pupal period of such nondiapause proportion of the pupae formed appear to enter individuals is lengthened by the low temperature. It diapause from which they do not emerge until the is also possible to find out, by inspection with a following rainy season.

21 Adults hosts; in the Sudan, Ipomoea cordofana (Convolvulaceae). T h e f e m a l e H. armigera is a stout-bodied moth, 18 Bhatnagar and Davies (1978) recorded 50 spe• to 19 mm long, with a wing span of 40 mm. The male cies of crop plants and 48 species of wild and weed is smaller, wing span 35 mm. Forewings are pale species of plants for H.armigera at Patancheru, brown with marginal series of dots; black kidney- Andhra Pradesh, whereas 96 crops and 61 weeds shaped mark present on the underside of forewing; and wild species have been recorded elsewhere in hind wings lighter in color with dark-colored patch India. The most important carryover weed hosts in at the apical end. Tufts of hairs are present on the the hot summer season are Datura metel, Acan- tip of the abdomen in females. thospermum hispidum, a n d Gynandropsis gynan- The female moth is the longer lived. In theUnited dra for H. armigera, H. assulta, a n d H. peltigera. States, the average figures for H. zea are 7.5 to 14.0 days for males and 9.25 to 18.0 for females, the longest lived male surviving for 19.5 days and the Preference for Oviposition female for 38 days. In South Africa, males lived for 1 to 23 days (average 8.7) and females 5 to 28 (aver• and Feeding age 13.5). The length of life is greatly affected by the availability of food, in the form of nectar or its The preferred host plants for oviposition by H. equivalent; in its absence, the female fat body is armigera were studied by Vijayakumar and Jayaraj rapidly exhausted, and the moth dies when only 3 to (1981) and found to be, in descending order, 6 days old. This explains why moth activity is large• pigeonpea, field bean, chickpea, tomato, cotton, ly confined to the flowering phase of the crops. chillies, mung bean, and sorghum. A mean of 40.3 The moths copulate about 1 to 4 days after emer• eggs per plant was observed on pigeonpea (Table gence from the pupa, but only if they have fed on 2). Reddy (1973) and Loganathan (1981) reported nectar. They may lay infertile eggs before mating, similarly that pigeonpea was the preferred host for but mating stimulates oviposition. The moths nor• oviposition. Hillhouse and Pitre (1976) reported that mally remain inactive on the plants during the day; H. zea a n d H. virescens preferred cotton for ovipo• most activity is usually between sundown and dark, sition, while Parsons et al. (1937) reported that when they begin by feeding from nectaries or chickpea was most attractive for oviposition. insect honeydew or drops of moisture on their host The feeding preference of H. armigera was, in plants. descending order, pigeonpea, field bean, cotton, sunflower, sorghum, chickpea, mung bean, urd bean, and tomato. Chillies were not selected for feeding in the multiple-choice test (Table 2). A Host Plants mean of 16.9 larvae per three plants was observed on pigeonpea grown as a border crop around cot• ton, but the cotton recorded only 4.05 larvae (Table Heliothis can breed on a wide range of plants, and 3) during the September-February season (Vijaya• cotton is not the most favored. The crops attacked kumar and Jayaraj 1981). in many countries are maize, sorghum, oats, barley, pearl millet, chickpea, pigeonpea, cowpea, peas, various beans, cotton, sunflower, safflower, tobacco, tomato, brinjal, cucurbits, sweet potato, Food Consumption and Utilization groundnut, flax, citrus, lucerne, sunnhemp, cape gooseberry, potato, etc. From an ecological point of view, the rates of diges• There are various wild host plants recorded in tion and conversion of food by the most destructive South Africa, of which the most important are A cal- instars might serve as a reasonably precise esti• ypha segatalis (Euphorbiaceae) Amaranthus thun- mate of food utilization during the whole larval bergii (Amaranthaceae), Malvastrum period (Waldbauer 1968). Dhandapani and Bala- tricuspidatum (Malvaceae), Nicandra physaloides subramanian (1980a) studied the food utilization of (Solanaceae), Sonchus oleraceus a n d x a n t h i u m H. armigera from the third to the last instar larvae, pungens (Compositae). In Tanganyika, Portulaca using chickpea, pigeonpea, lablab, cotton, tomato, oleracea (Portulacaceae) and Tridax procumbens sorghum, maize, and sunflower as hosts. Total food (Compositae) are mentioned as important wild consumed was most in cotton and least in sun-

2 2 Table 2. Oppositional and feeding preference of H. armi g e r a I n m u l t i p l e - c h o i c e last o f h o s t p l a n t s ( m e a n o f t h r e e o b s e r v a t i o n s ) .

No. of eggs % o f No. of larvae % of larvae M o s t p l a n t l a i d / p l a n t oviposition f e e d i n g f e e d i n g

C o t t o n 1 7 . 0 1 0 . 7 3 . 7 1 8 . 4 (4.3)a ( 2 . 0 ) P i g e o n p e a 4 0 . 3 2 5 . 5 6 . 7 3 3 . 3 ( 6 . 3 ) ( 2 . 7 ) F i e l d b e a n 3 0 . 0 1 9 . 0 4 . 0 2 0 . 0 ( 5 . 5 ) ( 2 . 1 ) T o m a t o 1 9 . 3 1 2 . 2 0 . 3 1.7 ( 4 . 4 ) ( 0 . 9 ) M u n g b e a n 8 . 7 5 . 5 1 . 0 5 . 0 ( 3 . 0 ) ( 1 . 2 )

C h i l l i e s 1 1 . 0 7 . 0 0 . 0 0 . 0 ( 3 . 2 ) ( 0 . 7 ) C h i c k p e a 2 4 . 0 1 5 . 2 1 . 0 5 . 0 ( 4 . 9 ) ( 1 . 2 ) S o r g h u m 8 . 0 5 . 1 1 . 3 6 . 7 ( 2 . 6 ) ( 1 . 3 ) U r d b e a n 0 . 7 3 . 3 ( 1 . 0 ) S u n f l o w e r 1 . 3 6 . 7 ( 1 . 3 )

L S D ( P = 0 . 0 5 ) 0 . 7 3 0 . 3 0

Source: Vijayakumar and Jayaraj (1981). a . Numbers in parentheses are square-root transformati o n s .

flower. Approximately 80% of the larval food was tional interest, since this index measures the rate at consumed during the last instar stage and was which nutrients enter the digestive system. Several again most in cotton and least in sunflower. How• earlier workers have found that the dry-weight CIs ever, larval weight was maximum in lablab. were always higher than the corresponding fresh- weight CIs, because the insects contained a lower percentage of dry matter than their food. On each Consumption Index host plant, the CI values, both on dry-weight and fresh-weight basis, were highest in the third-instar The fresh-weight consumption index (CI) is gener• larvae and gradually decreased in each subse• ally taken as a measure of the behavioral response quent larval stage, indicating that the nutritional of insects towards the food (Waldbauer 1968). In requirement of the earlier instars is probably higher. the case of H. armigera, this index was highest in cotton and least in chickpea. Dhandapani and Balasubramanian (1980a) observed, in general, a Growth Rate direct correlation between the succulence of host plants and the feeding rate of the larvae (Spear- The relative growth rate of H. armigera w a s m a x i • man's rank correlation coefficient [rs]= 0.6666*). mum in sunflower and minimum in sorghum (Dhan• The dry-weight CI was higher in maize, probably dapani and Balasubramanian 1980a). As observed because of more dry matter. The CI calculated by Premkumar et al. (1977), more food consumed based on dry weight of food and fresh weight of does not necessarily give highergrowth rates. On a larva was highest in maize. This finding is of nutri• fresh-weight basis, the CI was maximum in cotton,

2 3 Table 3. Population of H.armigera larvae on pigeonpea border crop around main crop o f c o t t o n ( m e a n o f t h r e e observations).

P e r i o d Mean larval population on M o n t h W e e k P i g e o n p e a C o t t o n M e a n

O c t o b e r 3 2 . 3 4 . 7 7.0 (2.6)a ( 1 . 5 ) ( 2 . 1 ) O c t o b e r 4 1 1 . 7 5 . 3 8 . 5 ( 3 . 4 ) ( 2 . 3 ) ( 2 . 9 ) N o v e m b e r 1 1 2 . 0 4 . 3 8 . 2 ( 3 . 5 ) ( 2 . 1 ) ( 2 . 8 ) N o v e m b e r 2 2 7 . 3 9 . 0 1 8 . 2 ( 5 . 2 ) ( 3 . 0 ) ( 4 . 1 ) N o v e m b e r 3 1 8 . 3 5 . 3 1 1 . 8 ( 4 . 3 ) ( 2 . 3 ) ( 3 . 3 )

N o v e m b e r 4 2 0 . 3 4 . 7 1 2 . 5 ( 4 . 5 ) ( 2 . 2 ) ( 3 . 4 ) D e c e m b e r 1 1 7 . 0 4 . 0 1 0 . 5 ( 4 . 1 ) ( 2 . 0 ) ( 3 . 1 ) D e c e m b e r 2 2 5 . 3 3 . 3 1 4 . 3 ( 5 . 0 ) ( 1 . 8 ) ( 3 . 4 ) D e c e m b e r 3 2 4 . 7 3 . 0 1 3 . 8 ( 5 . 0 ) ( 1 . 7 ) ( 2 . 6 ) D e c e m b e r 4 1 7 . 7 2 . 0 9 . 8 ( 4 . 2 ) ( 1 . 4 ) ( 2 . 8 ) J a n u a r y 1 4 . 7 1 . 0 2 . 8 ( 2 . 1 ) ( 1 . 0 ) ( 1 . 5 )

M e a n 1 6 . 9 4 . 0 ( 4 . 0 ) ( 1 . 9 )

LSD ( P = 0 . 0 5 ) P e r i o d 0 . 3 2 C r o p 0 . 1 4 Period x Crop 0 . 4 6

Source: Vijayakumar and Jayaraj (1981). a. Figures in parentheses are square-root transform a t i o n s .

but the growth rate was lower. This may be due to dry-weight basis; however, on a fresh-weight basis, the presence of aldehydes and cyclopropenyl fatty approximate digestibility was maximum in acids in cotton (Chan et al. 1978). The dry-weight sunflower-reared and minimum in maize-reared CI was higher on maize, but this does not guarantee larvae (Dhandapani and Balasubramanian 1980a). a nutrient intake qualitatively or quantitatively ad e • Soohoo and Fraenkel (1966) reported that plants quate to support growth at the normal rate. The dry with thick structural carbohydrates encompassing matter ingested may be deficient in a nutrient or the individual cells are less digestible because of may be less digestible than the usual food (Wald- the physical barrier to mechanical and enzymatic bauer 1962). activity within the insect. The lower digestibility might also be due to a nutrient deficiency or nut• rient imbalance (Waldbauer 1962). Digestibility Tomato was well digested by the larvae, but resulted in poor growth, probably because the rate For H. armigera, the approximate digestibility (AD) of ingestion was so low that most of the food was of tomato was higher than that of sunflower on a used for body maintenance rather than growth. In

2 4 maize, on a dry-weight basis, the rate of consump• younger insects is generally higher per unit body- tion was high whereas the digestibility was com• weight than it is in later stages, a smaller portion of paratively low, resulting in low utilization. Possibly the digested food is channeled into tissue growth, the combination of low protein and high dry matter more of.it being used in maintenance. However, accounts for the low utilization. In general, the AD older larvae have a lower metabolic rate than value was highest in third-instar larvae and gradu• younger ones, and hence more of the digested food ally decreased in each subsequent larval stage. is available for conversion to body tissue. The decrease might have been due to the fact that young larvae are more selective feeders and choose more digestible, nutritious parenchymat• Effect of Host Plant on ous tissues of the food than older larvae, which Development and Reproduction apparently feed more indiscriminately.

Dhandapani and Balasubramanian (1980b) stu• Utilization of Food died the effect of eight species of host plants on t h e biology and reproduction of H. armigera. The e g g The efficiency of conversion of ingested food (ECI) stage ranged from 2.9 to 4.3 days on different food was highest in pigeonpea and lowest in sorghum plants. This is in agreement with the duration (2 to 5 on a dry-weight basis, while on fresh-weight basis, days) reported by Ewing et al. (1947), Srivastava it was maximum in sunflower and minimum in cot• and Saxena (1958), Hsu et al. (1960), Reed (1965), ton (Dhandapani and Balasubramanian 1980a). Continho (1965), and Singh and Singh (1975). The The ECI values did not remain constant during larval period ranged from 17 to 20 days. The min• larval development, but varied among instars. The imum and maximum were with pigeonpea and changes among instars might be influenced by the tomato, respectively (Dhandapani and Balasubra• digestibility of food, its nutritional value, and the manian 1980b). According to Minanandana (1964), level of nutrient intake. The dry-weight ECI possibly it was 19 and 16 days on pigeonpea and tomato. reflected better the balance of energy than the Singh and Singh (1975) observed 8 to 12 days on fresh-weight ECI. In cotton, the ECI declined with tomato and they reported that the deviation in larval larval age, both on a dry and fresh-weight basis. period might be due to the climatic conditions. In The indiscriminate feeding of older larvae and the maize and cotton, larval period was 18 and 18.3 greater energy spent for maintenance could days. Pretorius (1976) has also noted 17.4 and 18.2 a c c o u n t for this. days in maize and cotton respectively. The total larval duration was 21, 15, 24, and 19 days when The efficiency of conversion of digested food larvae were fed on cotton, soybean, tomato, and (ECD) was maximum in pigeonpea and minimum in corn respectively (Doss 1979). The weight of the sorghum on a dry-weight basis; on a fresh-weight sixth-instar larvae was significantly higher on cot• basis, it was highest in maize and lowest in lablab. ton (700 mg) than on sunflower, field bean, pigeon• As reported by Soohoo and Fraenkel (1966) in the pea, chickpea, and maize, which ranged from 598 c a s e of Prodenia eridania, the high ECD might be to 626 mg. The weight was reduced considerably due to the high nutritional value of the food and when larvae were reared on tomato (376 mg) and faster growth of the larvae. The fresh-weight ECD sorghum (390 mg) (Vijayakumar and Jayaraj for sorghum, maize, and sunflower was two to three 1981). The difference in larval period and weight times higher than the corresponding dry weight observed among hosts might be due to differential ECD. This probably reflects a high rate of retention nutritional status of the host. of the small amount of water taken in with the food and the storage of metabolic water obtained by the The pupal stage ranged from 10.5 to 13.6 days, oxidation of carbohydrates as reported in many being minimum on pigeonpea and maximum on insects (Waldbauer 1968). sorghum, maize, and sunflower. The weight of the In general, the ECD values were low during the pupae and percentage of pupae and moths formed third instar and gradually increased in the last were higher with cotton food material, lower with instar. This increase of ECD during larval develop- sorghum (Pretorius 1976; Dhandapani and Bala• ment has an inverse relationship to the approxi- subramanian 1980b; Vijayakumar and Jayaraj mate digestibility (AD). As noted earlier, young H. 1981). armigera larvae digested their food better than H. armigera adults from larvae fed on soybean older larvae, but since the respiratory rate of and cotton lived longer than those fed on tomato

2 5 and corn. The preoviposition period ranged from increase in numbers (1.16), and weekly multiplica• 2.5 to 3.4 days on different hosts; the oviposition tion (2.81 times) were recorded for cotton, and period, from 6.5 to 9.8 days. According to Sharma minimum values (140.6, 0.12, 1.13, and 2.80 (1978) the fecundity ranged from 584 to 1501 eggs respectively) were observed for tomato-reared in pigeonpea. Ewing et al. (1947), Christidis and insects. The mean length of the generation was Harrison (1955), and Hsu et al. (1960) recorded highest in sunflower (43.2 days) and lowest in that a female laid 500 to 3000 eggs with an average pigeonpea (38.1 days). in excess of 1000 eggs. A maximum of 1265 and On all hosts, the population on reaching a stable 1251 eggs were observed on cotton by Pretorius age distribution, was comprised approximately of (1976) and Vijayakumar and Jayaraj (1981). The 99% of immature stages. Thus the maximum con- number of eggs per female ranged from 387 to tributon towards the stable age distribution was 1346 eggs on different hosts (Dhandapani and made by the immature stages. Balasubramanian 1980b). The fecundity varied Significant correlations existed with the follow• because of nutritional qualities of various diets. ing: consumption index (fresh-weight) with innate Pretorius (1976) found that the ratio of total female capacity for increase in numbers (rm) and finite births in two successive generations was greater rate of increase (λ); growth rate with the net repro• on cotton food material. Based on percentage and ductive rate (Ro), weight of pupae, and percentage weight of pupae and number of moths formed, Pre• of pupae and moths formed. A positive correlation torius (1976) concluded that cotton leaves were was found between weight of the pupae and innate the most suitable host. Of the hosts tested by Dhan • capacity for increase; percentage of moths and dapani and Balasubramanian (1980) cotton bolls innate capacity for increase; net reproduction rate were found to be the most suitable for reproduction and innate capacity for increase; ECI and ECD on a and development; sorghum and tomato, the least dry-matter basis; and moisture percentage of host suitable. However, the presence or absence of plant and fresh-weight consumption index (Dhan• secondary plant substances that act as feeding dapani and Balasubramanian 1980b). deterrents or stimulants were not studied by these Bilapate et al. (1979), studying the population authors to determine the behavioral mechanism dynamics of H. armigera on sorghum, pigeonpea, that decides the host selection. and chickpea, found that pupal mortality was high (24%) because of parasitism and unknown causes in sorghum during August-September. The positive Life Tables value of the trend index (4.5) indicated that the mortality factors operating during this period were Life tables were worked out for H. armigera on eight not effective in causing decline in population. Pupal different hosts under laboratory conditions (Dhan• mortality resulting from failure to complete devel• dapani and Balasubramanian 1979,1980c, 1981 a, opment or inability of the adult to emerge was 45% 1981b). The highest survival from egg to adult in pigeonpea during October-November, but the emergence was noted on cotton (84 adults) and mortality factors during this period were ineffective lowest on sorghum (70 adults). Survival of insects in suppressing the pest population in pigeonpea. A on a food is commonly used as an indication of larval parasite Campoletis chlorideae w a s alone nutritional adequacy of the food for the insect. Mor• responsible for reducing the population on chick- tality in the larval stage occurred due to virus dis• pea during November-December. The negative eases. The highest mortality was observed during value of the trend index (0.051) indicated that the pupal formation, when the larvae struggled to mortality factors during winter were dominant in escape from their larval skins, the delicate cuticle reducing the pest population in chickpea. broke open, exposing their internal organs, and the insects subsequently died. On some hosts such as tomato and chickpea, mortality was observed in References early sixth-instar larvae. ANONYMOUS. 1977. Studies on the occurrence and The first female mortality after emergence control of cotton boll worms in the region of Honon p r o • occurred early (on the seventh day) on pigeonpea vince. Acta Entomologica Sinica 20:141-146. and late (tenth day) on cotton and maize. The maxi• mum net reproductive rate (537.0), innate capacity BEEDEN, P. 1974. Boll worm oviposition of cotton in for increase in numbers (0.15), finite rate of Malawi. Cotton Growing Review 5:52-61.

2 6 BHATNAGAR. V.S. 1980. A report on research on the DHANDAPANI, N., and BALASUBRAMANIAN, M. Heliothis complex at ICRISAT (India) 1974-79. Presented 1 9 8 0 c . Life table for the gram pod borer, Heliothis armig• at the All India Workshop on Consolidation of Pest M a n • era Hbn. on three pulse crops. Proceedings, Indian agement Recommendations and Guidelines of Research. Academy of Sciences (Animal Science) 89:575-578. 24-26 Apr 1980, Udaipur, India.

DHANDAPANI, N., and BALASUBRAMANIAN, M. BHATNAGAR, V.S., and DAVIES, J.C. 1978. F a c t o r s 1981a. Growth of population of Heliothis armigera H b n . affecting populations of gram pod borer, Heliothis armig• on maize and sorghum. Indian Journal of Ecology (In era (Hubner) in the period 1974-77 at Patancheru press). (Andhra Pradesh). Presented at the Oriental Entomol o g y Workshop on Population Ecology in Relation to Insec t s o f DHANDAPANI, N., and BALASUBRAMANIAN, M. Economic Importance, 18-20 Jan 1978, Bangalore, India. 1981b. Life table studies of gram pod borer, Heliothis armigera (Hubner) on tomato. Indian Journal of Entomol• BILAPATE, G.G., RAODEO, A.K., and PAWAR, V.M. ogy (In press). 1979. Population dynamics of Heliothis armigera H u b n e r in sorghum, pigeonpea and chickpea in Marathwada. DOSS, S.A. 1979. Effect of host plants on some biologi• Indian Journal of Agricultural Sciences 49:560-566. cal aspects of bollworm, Heliothis armigera ( H u b n e r ) Lepidoptera, Noctuidae. Zeitschrift fur Pflanzenkra n k - BRAZZEL, J.R., NEWSOM, L.D., ROUSSEL, J.S., heiten und Pflanzenschutz 86:143-147. LINCOLN, C., WILLIAMS, F.J., and BARNER, G. 1 9 5 3 . Bollworm and tobacco budworm as cotton pests in EWING, K.P., PARENCIA, C.R., and IVY, E.E. Louisiana and Arkansas. Louisiana Agricultural Expe r i • 1947. Cotton insect control with benzene hexachloride, ment Station Technical Bulletin 482, Baton Rouge, L a , alone or in mixture with DDT. Journal of Economic E n t o • USA. mology 40:374-381.

CHAN, B.G., WAISS, A.C., BINDER, R.G., and FIFE, L.C., and GRAHAM, H.M. 1966. Cultural control ELLIGER, C.A. 1978. Inhibition of lepidopterous larval of overwintering bollworm and tobacco budworm. Journ a l growth by cotton constituents. Entomologia Experime n t a - of Economic Entomology 59:1123-1125. lis et Applicata 24:94-100. HARRELL, E.A., PERKINS, W.D., and MULLINIX, B.G. CHRISTIDIS, B.G., and HARRISON, G.J. 1955. C o t • 1979. Effects of temperature, relative humidity, and air ton growing problems. New York and London. McGraw- velocities on development of Heliothis zea. Annals of the Hill. 6 3 3 pp. Entomological Society of America 72:222-223.

COAKER, T.H. 1959. Investigations on Heliothis armig• HILLHOUSE, T.L., and PITRE, H.N. 1976. Oviposition era (Hb.) in Uganda. Bulletin of Entomological Researc h by Heliothis on soybeans and cotton. Journal of Eco• 50:487-505. nomic Entomology 69: 144-146.

CONTINHO, S.A. 1965. Polyphagous larvae—H e l i o t h i s HSU, MING-SHIA, CHANG, GUANG-SHIO, and CHU armigera a n d Heliothis peltigera in the Cape Verde HUNG-FU. 1960. A study on cotton boll worm, Heliothis Islands. Garcia de Orta 11.593-599. armigera (Hubner) (Lepidoptera: Noctuidae). Acta Oeco- nomico Entomologica Sinica 1:18-30. DHANDAPANI, N., and BALASUBRAMANIAN, M. 1979. Life tables for the gram pod borer, Heliothis armig• LINCOLN, C. 1972. Distribution, abundance and control era Hubner (Lepidoptera, Noctuidae) on cotton. Journal of Heliothis species in cotton and other host plants. South• of Entomological Research 3:186-190. ern Cooperative Series Bulletin 19. 92 pp.

DHANDAPANI, N., and BALASUBRAMANIAN, M. LOGANATHAN, M. 1981. Studies on ecology and 1 9 8 0 a . Consumption and utilization of different food effect of host plants on the susceptiblity of larva e of H e l i o - p l a n t s by Heliothis armigera (Hubner) (Noctuidae, Lepi• this armigera (Hubner) to insecticides. M.Sc. (Ag.) Thesis, doptera). Entomon 5:99-103. Tamil Nadu Agricultural University, Coimbatore, India.

DHANDAPANI, N., and BALASUBRAMANIAN, M. MINANANDANA, N. 1964. Studies on biology and host 1980b. Effect of different food plants on the development r a n g e of Heliothis armigera (Hubner) (Lepidoptera: Noc• and reproduction of Heliothis armigera (Hbn.) Experientia tuidae). M.Sc. (Ag.) thesis, Madras University, Mad r a s , 36:930-931. India.

2 7 NEUNZIG, H.H. 1964. Wild host plants of the corn ear- SINGH, H., and SINGH, G. 1975. Biological studies on worm and the tobacco bud worm In Eastern North Carol• Heliothis armigera (Hubner) in the Punjab. Indian Journal ina. Journal of Economic Entomology 56:135-139. of Entomology 37:154-164.

NIKISHINA, E.S. 1980. The diapause of the cotton boll- SOOHOO, C.F., and FRAENKEL, G. 1966. The con• worm and the phenology of cotton. Zashchita Rasteni 6: sumption, digestion and utilization of food plants by poly- 37. phagous insect, Prodenia eridania (Cramer). Journal of Insect Physiology 12: 711 -730. PARSONS, F.S., HUTCHINSON, H., and MARSHALL, J. 1937. Progress reports from experimental stations, SRIVASTAVA, A.S., and SAXENA, H.P. 1958. Tissue season 1936-37. Empire Cotton Growing Review 8, Lon- borers and problems of their control. Pages 109-114 in don, UK. 129 pp. Proceedings, Entomology Research Workers Confer• ence, Simla, India. PATEL, R.C., PATEL, J.K., PATEL, P.B., and SINGH, R. 1968. Mass breeding of Heliothis armigera .Hbn. lndian VIJAYAKUMAR, A., and JAYARAJ, S. 1981. Studies Journal of Entomology 30: 272-280. on the food plant ecology of Heliothis armigera (Hubner) (Lepidoptera, Noctuidae). Indian Journal of Agricultural PATEL, R.C., PATEL, R.M., MADHUKAR, B.V.R., and Sciences (In press.) PATEL, R.B. 1974. Oviposition behavior of Heliothis armigera in cotton hybrid-4. Current Science 43:588-589. WALDBAUER, G.P. 1962. The growth and reproduction of maxillectomized tobacco hornworms feeding on nor• PEARSON, E.O., and DARLING. R.C.M. 1958. The mally rejected non-solanaceous plants. Entomologia insect pests of cotton in tropical Africa. London, UK: Experimentalis et Applicata 5:147-158. Empire Cotton Growers and Commonwealth Institute of Entomology. 355 pp. WALDBAUER, G.P. 1968. The consumption and utiliza• tion of food by insects. In Advances in Insect Physiology 5 PREMKUMAR. M., DALE, D., and NAIR, M.R.G.K. (ed. M. Rockstein). New York, USA: Academic Press. 1977. Consumption, digestion and utilization of food by larvae of Spodoptera litura F. (Lepidoptera: Noctuidae). WILCOX, J., HOWLAND, A.F., and CAMPBELL, R.E. Entomon 2: 7-10. 1956. Investigations on the tomato fruit worm, its sea• sonal history and methods of control. U.S. Department of PRETORIUS, L.M. 1976. Laboratory studies on the Agriculture Bulletin 1147, Washington DC, USA. 47 pp. developmental reproductive performance of Heliothis armigera on various food plants. Journal of the Entomo• logical Society of South Africa 39: 337-343.

REDDY, K.V.S. 1973. Studies on the gram caterpillar, Heliothis armigera (Hb.) (Lepidoptera, Noctuidae) with special reference to its biology, host preference and esti• mation of loss in redgram. Ph.D. Thesis, University of Agricultural Sciences, Bangalore, India.

REED, W. 1965. Heliothis armigera (Hb.) (Noctuidae) in Western Tanganyika. I. Biology with special reference to the pupal stage. II. Ecology and natural and chemical control. Bulletin of Entomological Research 56:117-125.

ROOME, R.E. 1975. Activity of adult Heliothis armigera with reference to the flowering of sorghum and maize in Botswana. Bulletin of Entomological Research 65: 523- 530.

SHARMA, S.K. 1978. Studies on the biology and extent of damage of gram pod borer, Heliothis armigera (Hubner) (Lepidoptera, Noctuidae). M.Sc. (Ag.) Thesis, Haryana Agricultural University, Hissar, India.

2 8 Studies on the Biology of Heliothis Spp in Sudan

D.S. Hackett and A.G. Gatehouse*

Abstract

Tethered flight behavior of female Heliothis armigera (Hb) was studied in the laboratory, using methods adapted for moths or a novel automated technique. Flight performance increased from day 1 to day 4, and feeding had the effect of stimulating oviposition and flight, though long flight was inhibited shortly after feeding. Full flight performance occurred in 4-day-old females under conditions suggesting the presence of a reproductive delay; 49% of a group of 122 females flew for more than 2 hours. Ovipositing females tended not to fly persistently. Factors affecting the duration of the prereproductive period were probably larval diet and temperature in the early adult stage. These phenomena are consistent with H. armigera being a facultative migrant. Diapause occurred in H. armigera pupae when larvae, prepupae, and pupae were exposed to cool (22°C). short-day (12 h light) conditions in the laboratory. After a suitable period at low temperature, certain pupae remained undeveloped after.transfer to high temperature (34° C) for 80 days, and then developed and emerged in response to a drop in temperature. This could provide a mechanism to bridge the dry season and emerge after the first rains. H. fletcheri (Hdwck) underwent prolonged diapause, from the end of the rainy season until the following rains. The implications of these findings tor management of Helio• this are discussed, and suggestions made for further study.

Recently a large part of the Gezira cotton pest insecticide. In order to kill susceptible hatching complex, chiefly consisting of Heliothis armigera larvae of Heliothis, it has been necessary to scout (Hubner) and white fly Bemisia tabaci (Gennadius), the cotton crop frequently and respond with sprays has been successfully controlled by nonpersistent when and where necessary (Joyce 1978). Research effort has been put into studying patterns of oviposition and the origin of Heliothis adults, *Department of Applied Zoology, University College of North Wales, Bangor, Gwynnedd, Wales, UK. emphasis being given to the mobility of insects in

International Crops Research Institute tor the Semi-Arid Tropics. 1982. Proceedings of the International 2 9 Workshop on Heliothis Management 15-20 November 1981, Patancheru, A.P., India. wind systems (Bowden and Gibbs 1973; Joyce was cemented to the thorax with melted beeswax 1976; Schaefer 1976; Topper 1978; Haggis 1978, in the period from 1 hour to 0.5 hours before dusk or 1981). lights off. Flight testing of moths of different ages Migratory flight in many insects is a prereproduc- was conducted in the period 0.5 hours after lights tive phenomenon (Johnson 1969), and therefore off or dusk until 2 hours later. The test consisted of some workers have dissected light-trap catches of supporting the wire mountings on a horizontal bar, H. armigera in order to detect changes in age and initiating flight by removing tarsal contact, and ti m • reproductive state of females that could indicate ing flight duration until wing beating stopped or wa s migration (Bowden and Gibbs 1973; Morton et al. much reduced in amplitude. Each moth was tested 1981; Roome, unpublished1 ). Similar assumptions for 30 minutes or over five successive flights, have been made for Heliothis zea (Boddie), e.g. whichever occurred sooner. The duration of the Callahan et al. (1972). The current study investi• longest flight within the 30-minute test period was gated changes in the flight behavior of H. armigera recorded. Observations were carried out under dim females in the laboratory in relation to age and red light to keep disturbance to a minimum. reproductive state, which may indicate when The second technique, termed the flight swing migration may occur. technique, was based on the first, except that flight A cotton closed season is enforced in the Gezira started spontaneously in the dark, and flight dura• from April to June, and the area of alternative host tion was measured automatically. The moth was plants for H. armigera in this dry season is quite tethered by a harness to a wire support connected restricted. Observations by Balla (1970, 1973) in to a pivot. A mercury switch or photocell activated Sudan suggest that very low proportions of pupae by the swing signaled an event recorded when diapause at the end of the growing season. This flight started or stopped. When inactive, the moth contrasts with earlier work by Cowland (1935) in rested on a foam plastic ball or paper-covered which high percentages of diapause occurred from roller, which allowed eggs laid overnight to be October onwards. This paper summarizes work c o u n t e d . undertaken for a doctoral study on diapause and flight in Heliothis in Sudan (Hackett 1980). Diapause Studies Materials and Methods More than 1000 pupal periods of H. armigera in the Flight Studies field in Sudan were measured from August until the end of November in 1976,1977, and 1978. Pupae were derived from larvae collected from or reared H. armigera adults were derived from larvae col• on groundnut, sorghum, cotton, or artificial diet, a n d lected in the field, chiefly from sorghum, and were held in a Stevensons screen or netting-walled allowed to feed on sorghum or on artificial diet. insectary. In 1978, insect material collected from Alternatively, insects were derived from first- sesame resulted in a high percentage of diapause generation insects in culture on artificial diet. Ag e s in the first generation, in late September. The spe• of moths refer to the night of emergence as night cies identified from the nondiapause insects was zero. Insects at Bangor were kept under 26°C, 70% Helicoverpa (Heliothis) fletcheri (Hardwick) (Hack• RH, and 13-hour light conditions; those in Sudan ett and Gatehouse 1979). As field infestations of H. were kept under ambient conditions either in a armigera were difficult to secure from November laboratory without airconditioning or a netting- onwards, insects were cultured under 26°C, 75% walled insectary. Where mating was necessary, RH, and 13-hour daylength conditions. Since dia• females were caged on night 3 with males 2 to 7 p a u s e in H. armigera has been found to be induced days old and dissected after flight testing. by low temperatures and short day lengths (Komar- Two techniques involving tethering were deve- ova 1959; Roome 1979), possible induction condi• loped for use with H. armigera females. The first, tions (22°C and 11.5 hr daylength) were modeled termed static tethered flight, was based on the on January in the Gezira, which is the coldest method of Dingle (1965). After CO2 anesthetization month with the shortest daylength. of each moth, a small foil bracket on the tip of a wire The dry-season conditions after January

*R.E. Roome, 1972, Report of the Drylands Farming Research become hotter, and then temperatures drop when Team, Botswana, Entomologists' Report (or 1971 -1972. the rainy season begins. Initially, insects resulting

30 from induction conditions were transferred to 26°C experiment 1 may have been due to different larval to demonstrate their ability to remain undeveloped diet or environmental conditions during the tests. at higher temperatures. Subsequently, pupae after more than 2 months in diapause were subjected to Effect of Food on Flight in Sexually a high temperature (34°C) and then to a lower one Immature Females (26°C) to simulate passing the dry season. The criterion for determining diapause was the pres• In these experiments 1 - and 2-day-old moths were ence of larval eyespots, as used by Wilson et al. supplied with 10% sugar or honey as food on each (1979), for example. Nondiapause pupae lost their night in static tethered flight and on alternate nights eyespots on day 2 at 26°C (control conditions). between flight-swing tests. Since other workers Pupae formed at 22°C were examined daily to note had shown that feeding stimulates reproduction in the loss of eyespots. Diapause pupae could be Heliothis and that oviposition would be heavy by separated safely from nondiapause pupae on day night 4, an experiment was set up to examine the 12 at this temperature. effect of starvation on flight by 1 - and 2-day-old female moths. The study was carried out in two parts. In part A, Results starved moths were flown on night 1 only, night 2 only, or fed 10% sucrose on night 1 and then flown Flight Studies on night 2. In part B, a group of moths fed to reple• tion at 1600 hours on day 2, just before attachment Effect of Age on Flight in Female Moths to the flight swing, was compared with a starved group of the same age. Feeding on night 1 or on the Short flights of 1 minute or more were taken by afternoon of day 2 had no significant effect on flight females of all ages (Table 1); however, there was a performance on night 2, though there was some tendency for lower proportions of young females 1 indication that a small increase in long flight and 2 days old to take flights of longer duration, occurred in fed moths (Table 2). However, a further such as > 5 minutes and >30 minutes. A very low indication of an increase in long flight on night 2 proportion of females took flights of > 120 minutes compared with night 1 was detected. The timing of duration on the flight swing. The rather higher pro• long flight (>60 min) during night 2 was examined portion of females taking flights > 30 minutes in from part B. In starved moths, the majority of flights

Table 1. The effect of age on flight in H. armigera f e m a l e s .

Percentage of moths showing continuous flight for >1 min >5 min >30 min >120 min Experiment Experiment Experiment Experiment Age of moths 123 123 123 1 2 3

1 d a y 8 6 4 8 a 1 3 2 d a y s 91 59 100 84b 53 71 22y 0 16 4 4 d a y s 100 100 100 90 100 73 62z 15 36 9 6 d a y s 100 100 100 94 100 70 77 27 24 0

Experiment 1. Static tethered flight using unmated moths collecte d from sorghum in Sudan (n=23, 37, 21, and 17, for 1-, 2-, 4-, and 6-day-ol d females, respectively).

Experiment 2. Static tethered flight using unmated moths from F1 generation on artificial diet at Bangor (n= 17, 20, and 18, for 2-, 4-, and 6-day -old females respectively).

Experiment 3. Flight swing, using mated and unmated moths from ar tificial diet in Sudan (n=25, 44, and 17, for 2-, 4-, and 6-day-old females respe c t i v e l y ) .

Values followed by different letters indicate where significant differences occur (P<0.05).

31 Table 2. Effect of feeding on flight in 1- and 2-day - o l d H . armigera females.

Percentage of months showing flight duration of P a r t o f e x p e r i m e n t A g e F e e d i n g >5 min >30 min >60 min >120 min

A ( n = 4 5 ) 1 d a y S t a r v e d 89 33 8a 0 A+Ba (n=62) 2 days Starved 91 53 27b 9 A ( n = 2 4 ) 2 d a y s F e d n i g h t 1 96 58 29 20 B ( n = 3 9 ) 2 d a y s F e d a t 1 6 0 0 h r 97 59 41 18 o n n i g h t 2

Values followed by different letters indicate where sig nificant differences occur (P<0.05). a . Flight data for 2-day-old starved females from parts A and B (described in the text) were p o o l e d , a s n o s i g n i f i c a n t d i f f e r e n c e s i n a n y f l i g h t - d u r a tion category existed.

Table 3. Effect of feeding on timing of flight in 2- d a y - o l d H . armigera females.

Percentage of moths showing flight duration of > 6 0 m i n , s t a r t i n g > 6 0 m i n . s t a r t i n g E x p e r i m e n t before 2400 hr after 2400 hr

Starved (n= 40) 3 0 1 0 a F e d 1 0 % s u c r o s e a t

1600 hr on night 2 (n= 39) 1 1 3 1 b

Values followed by different letters indicate where si gnificant differences occur (P<0.05).

started before midnight; in the group fed at 1600 (1978). Moths were caged with males on night 3 hours, fewer moths flew for long periods before only, and flight-tested on nights 4 and 6 (1977) or midnight, but the situation was reversed after midnight 4 only (1978). The proportion of moths mating night (Table 3). was significantly different (P < 0.025) in the 2 years: 42.6% (n=61) in 1977 and 24.4% (n=164) in 1978. There was also a large difference in the pattern of Effect of Feeding on Oviposition in oviposition between the two years, both in the pro• 2-Day-Old Females portion of females ovipositing and in the number of eggs laid (Table 4). There were significant differ•

The flight-swing apparatus allowed eggs laid over• ences (Mann-Whitney U test) in the numbers of night to be counted. Feeding on night 1 significantly eggs laid by ovipositing 4-day-old mated versus (P <0.01) increased the proportion of females ovi• unmated females in 1977 (P < 0.01) and in 1978 (P positing on night 2 (43.5%, n=23),compared with < 0.05). By night 6, however, u n m a t e d a n d m a t e d starved moths (14.3%, n=63) or those fed at 1600 hr females in 1977 were laying similar numbers of on night 2 (9.2%, n=39). These results indicate that eggs. Both mated and unmated females laid more feeding affected subsequent oviposition, although eggs in 1977 than in 1978. in the short term there was no effect. In 1978, the lower percentage of females mating and ovipositing and the fewer eggs laid suggest that there was a delay in reaching reproductive Relationship between Mating, maturity. This conclusion was supported by a small Oviposition, and Flight number of unmated females subjected to the same feeding regime as those flight-tested, but kept indi• Mated and unmated females were tested on the vidually in cages. The proportion of these moths flight swing in 1977 and 1978 in Sudan. Adults were ovipositing rose from 11 % on night 4 to 89% on derived from larvae reared on artificial diet (1977) night 6; i.e., the insects were able to oviposit, but it or collected and fed to pupation on sorghum took longer for them to start.

32 Table 4. Oviposition by 4-and 6-day-old mated and un m a t e d H. armigera females on flight-swing apparatus In 1977 and 1978. a

P e r c e n t a g e Mean number of b Year and age Mated status ovipositing e g g s l a i d

c 1977 4 days M a t e d 100 (20) 296 (20)c 4 d a y s U n m a t e d 9 6 ( 2 6 ) 6 2 ( 2 5 ) 6 d a y s M a t e d 9 0 ( 1 0 ) 2 2 3 ( 9 ) 6 d a y s U n m a t e d 9 1 ( 1 1 ) 1 9 6 ( 1 0 )

1978 4 days M a t e d 5 7 ( 3 3 ) 4 4 ( 1 9 ) 4 d a y s U n m a t e d 3 6 ( 8 9 ) 9 ( 3 2 ) a . Proportions of 4-day-old mated females ovipositing we re found significantly different ( P < 0 . 0 5 ) between years, as were proportions of unmated oviposi t i n g f e m a l e s ( P < 0 . 0 1 ) b . Determined by subsequent dissection. c. n = numbers in parentheses.

Table 5. Flight performance of 4-day-old H.armigera females In relation to mating.

Percentage of moths showing flight duration of Year and status > 5 m i n > 3 0 m i n > 6 0 m i n > 1 2 0 m i n

1 9 7 7 Mated (n=19) 7 4 3 7 2 7 1 0 Unmated (n=25) 7 2 3 6 2 4 8 1 9 7 8 Mated (n=33) 9 7 8 1 6 3 4 8 Unmated (n = 89) 9 7 7 6 5 9 4 9

Since the percentage of mating in 1977 was oviposited. A significantly smaller proportion of greater than in 1978 and mating affected oviposi- ovipositing moths (31 %, n=51) gave flights of > 120 tion during night 4, flight data for mated and minutes duration compared with moths not ovi- unmated females were treated separately (Table positing (71 %, n=71; P < 0.05). The duration of the 5). No significant differences were found between longest flight by the 60 moths that flew for >120 mated and unmated females within years in any minutes was examined. Again ovipositing moths flight-duration category; however, comparison tended to fly for a shorter time than those not ovi• between years showed mated females to be signifi- positing (Table 6). cantly different in the > 30-minute (P< 0.05) and> 120-minute (P< 0.025) categories. Unmated females were similarly compared and found to be Diapause Studies significantly different (P< 0.05) in the long-flight categories (> 30 minutes). Mating therefore did not Less than 1 % of H. armigera pupae formed under significantly affect flight, but large differences in field conditions in Sudan had an extended pupal long-flight categories existed between years. period. The few slow-developing pupae that Since the proportion of moths ovipositing (and occurred were formed in cooler weather in numbers of eggs laid) was greater in 1977 than in November. The study was continued under con• 1978, the incidence of long flight was analyzed trolled conditions (Table 7). from 1978 data on 4-day-old females with respect Under the control conditions of 26°C and 13 to whether the moth oviposited or not. Similar data hours daylength, no diapause occurred (Treatment were not available from 1977, as nearly all moths 1). Control temperature and short (11.5 hr) day-

3 3 length also produced no diapause (Treatment 2). 11.5 to 12 hours (Treatment 6), incidence of dia• When the feeding part of the larval stage was main• pause further increased. Adults emerged earlier tained under low-temperature (22°C) short-day from pupae which had diapaused in treatment 4 conditions, and insects were transferred to control than in treatment 5 or 6, indicating a lower diapaus e temperatures at the prepupal stage, a very low intensity in treatment 4. percentage (ca 5%) of pupae diapaused (Treat• Pupae in diapause 80 to 82 days after median ment 3). The incidence of diapause was increased pupation from treatments 5 and 6 were subjected to to over 30% in pupae produced from larvae reared further treatments designed to test responses to under control temperature and daylength and rising soil temperatures such as occur during the transferred to 22°C at the prepupal stage (Treat• dry season in the Gezira. A group of 33 pupae was ment 4). When larvae as well as prepupae and taken from 22°C and subjected to a rising tempera• pupae were reared under low-temperature, short- ture regime to 34°C over a period of 5 days. A day conditions (Treatment 5), diapause increased control group of nine pupae was transferred at the to over 60%. When daylength was increased from same time to a different incubator at 22°C. The rising temperature regime stimulated 64% of the pupae to break diapause, develop, and emerge 9 to 22 days after the temperature rise started. T a b l e 6 . F l i g h t d u r a t i o n o f 4 - d a y - o l d t o m a t o H.armig- Twelve pupae remained in diapause, but one broke e r a I n r e l a t i o n t o o p p o s i t i o n . diapause and emerged on day 155 after pupation.

Percentage of moths The remaining pupae were examined on day 164 showing flight duration of and all were found to be still in diapause. On day 2 - 5 h r > 5 h ra 165, 79 days after first being exposed to 34°C, the pupae were transferred to 26°C to simulate a drop Not ovipositing 4 7 5 3 in the soil temperature at the start of the rainy ( n = 4 4 ) season in the field. All pupae broke diapause within Ovipositing 8 1 1 9 3 days and emerged 14 to 17 days after transfer. ( n = 1 6 ) Control pupae transferred from 22°C to the differ• ent incubator at 22°C all broke diapause and a. The longest recorded flight was 719 emerged 22 to 36 days after transfer. The close m i n u t e s . association of the period of emergence with the

Table 7. Occurrence of diapause In H. armigera pupae undar controlled conditions.

P u p a l p e r i o d Conditions of treatment range (days)

L a r v a Prepupa/pupa N o n d i a - D a y p u p a e P e r c e n t T r e a t m e n t T e m p D a y l e n g t h T e m p D a y l e n g t h p a u s e D i a p a u s e i n s p e c t e d diapausea ( ° C ) ( h o u r s ) < ° C ) ( h o u r s )

b 1 A (42) 2 6 1 3 2 6 0 1 1 - 1 4 3 0 B ( 2 7 ) 2 6 1 3 2 6 1 3 1 3 - 1 7 4 0 2 ( 4 4 ) 2 6 1 1 . 5 2 6 1 1 . 5 1 3 - 1 4 4 0 3 A ( 2 2 ) 2 2 1 1 . 5 2 6 0 1 3 . 1 4 4 0 B ( 4 7 ) 2 2 1 1 . 5 2 6 0 1 2 - 1 7 5 0 - 8 0 6 6 . 4 8 4 . 3 C ( 4 9 ) 2 2 1 1 . 5 2 6 0 1 3 - 1 8 8 3 4 6 . 1 4 ( 2 5 ) 2 6 1 3 2 2 1 1 . 5 2 1 - 2 6 3 4 - 7 9 1 2 3 2 B ( 7 6 ) 2 2 1 1 . 5 2 2 1 1 . 5 2 0 - 2 8 36-93C 1 2 6 0 . 5 6 ( 6 1 ) 2 2 1 2 2 2 1 2 2 9 39-91c 1 2 9 7 . 6

a . Presence of larval eyespots denoted diapause. b . Figures in parentheses denote number (n) in each treat m e n t . c. Upper limit not given as pupae subjected to furthe r treatments.

34 transfer to different incubators suggested that flight (to exhaustion on flight mills) in other Noctu i d s some factor associated with the equipment pro- (Koerwitz and Preuss 1964; Hwang and How 1966; vided a stimulus for diapause termination. Kishaba et al. 1967); stimulation of mating and An intended fourth treatment in which pupae in oviposition by food in Heliothis spp has also been diapause were to be exposed to 34°C by means of reported (Parsons and Marshall 1939; Callahan a more gradual rise in temperature failed to give 1958). In many insects, factors that stimulate results because of equipment malfunctioning. reproduction inhibit migration and vice versa (Kennedy 1961). In bugs, reductions of quantity or quality of food delay oviposition and stimulate Diapause in H. fletcheri migration (Dingle and Arora 1973; Kehat and Wyndham 1973; Rankin and Riddiford 1977). It is Observations on H. fletcheri were confined to likely, therefore, that feeding could affect migration insects maintained under field conditions in Sudan. in Heliothis through this mechanism, and further Pupae from larvae on sorghum or artificial diet were experiments with controlled feeding of older adults held in a Stevensons screen throughout. Ninety- are required. three pupae were formed in the last week of Sep• In this study, nonovipositing females 4 days old tember 1978. Twenty-four adults emerged from 1 showed the highest incidence of flight of more than October to 8 October, but the remaining 69 insects 2 hours' duration. This was associated with a lower diapaused until 1979, when 61 adults successfully percentage of mating on night 3 and with lower emerged over the period from 13 June to 6 August. oviposition on the night of testing. On the hypothe• This gave a median diapause pupal period of over sis that the lower incidence of mating occurring in 9.5 moths. 1978 was due to environmental conditions, the results on mating from both years were analyzed with respect to mean temperature calculated from Discussion 2-hourly thermograph readings over the first 2 days of the adult lives of each group of females. The Tethered flight tests indicated that there was an calculated mean temperature range was then increase in ability of insects to fly for a long dura• divided into five 1.6°C classes and the incidence of tion, correlated with age up to day 4. Several exam • mating associated with each class calculated ples of other Lepidoptera showing development of (Table 8). The data suggest that temperature sig• flight ability were given by Johnson (1969) and nificantly affected the proportion of females mating more recently by Sharp et al. (1975) and Leppla et (X2 =25.73; 4 d.f. P< 0.05). The response was an al. (1979). inverted U shape about the central temperature Feeding in young moths tended to inhibit long groups C and D 27.2°C to 30.39°C. Isely (1935) flight soon afterwards, but promoted flight and ovi - working on H. zea had also found a U-shaped position later. Feeding has been shown to promote response to temperature in the pre-oviposition

Table 8. Effect of temperature In early adult life o n m a t i n g I n H . a r m i g e r a f e m a l e s a n d p r e - o v i p o s i t i o n p e r i o d i n H . zes.

Heliothis armigera femalesa Heliothis zea femalesb Temperature Number of females Percent mating Number of Pre-oviposition c l a s s i n c l a s s on night 3 Temperature f e m a l e s p e r i o d ( ° C ) ( ° C ) ( d a y s )

A < 2 5 . 5 9 9 2 1 9 2 3 1 1 4 . 3 B 25.6-27.29 2 8 1 8 2 5 4 1 3 . 1 C 27.2-28.79 4 8 3 5 2 8 2 0 2 . 1 D 28.8-30.39 3 0 6 3 3 0 8 3 . 6 E > 3 0 . 4 2 7 1 8 3 1 1 3 5 . 6 a. Source: Hackett (1978). b . Source: Isely (1935)

3 5 period of females, with a minimum at 28°C. The tion that Cowland (1935) was, in fact, looking at this length of the pre-oviposition period in many insects species. The species composition of Heliothis in is of decisive importance in determining the extent the irrigated and rainfed areas of Sudan requires to which migration will take place (Caldwell 1974; further investigation. Gatehouse and Hall 1976; Dingle 1978). The rea• On the basis of the current study, which sug• son for the higher incidence of mating and oviposi- gested that migration and diapause in H. armigera tion (and reduced flight) in females in 1977 could are facultative, it would be unwise to define the then have been due to more favorable tempera• life-history strategy of the insect in oversimplified tures, since data from this year, all fell in the central terms. The contribution of diapause pupae versus classes B, C, and D. continuous generations to bridge the dry season Other factors, such as larval diet, could have will have to be investigated in more detail in the caused the differences in the insects between the 2 field, paying particular attention to soil tempera• years, as in 1977, insects were derived from artifi• tures. It may well be that both strategies are fol• cial diet, and in 1978 from sorghum. Callahan lowed to spread risk. The same may apply to adult (1962) suggested that larval diet affected fat com• migration; local as well as distant immigrants may position and possibly reproduction in H. zea, a n d occur in crops in a dynamic balance. Ovipositing Gross and Young (1977) found the pre-oviposition females or those already mated may also be rela• period in H. zea was affected by larval diet. tively mobile under some conditions, which could affect future monitoring or mating-suppression Long-duration flight, therefore, appears to be techniques. possible in H. armigera females under conditions which delay reaching reproductive maturity. It is quite likely that at the end of the rainy season mo t h movement into the Gezira is feasible, as is move• Acknowledgments ment southwards (Joyce 1976; Haggis 1978) when environmental conditions become less suitable for The authors would like to thank the Director of the reproduction with the approach of cool or exces• Gezira Agricultural Research Station, Wad Medani, sively hot weather. and Mr. J. Hobart, Applied Zoology Department, Tethered flight techniques using suitable appa• U niversity College of North Wales, Bangor, for pro• ratus on Noctuid moths may enable a model of viding facilities for this study. Thanks are also d u e migration to be developed, this aspect of biology to Mr. M. Honey, British Museum, for species identi• being otherwise inaccessible. If migrating insects fication; Professor Sayed el Bashir, University of could be characterized physiologically, then Khartoum, and Dr. El Tigani el Amin (GARS) for trapped specimens in the field could be dissected helpful discussions in Sudan; and Professor R.J.V. or kept alive for observation, to distinguish migrants Joyce and R.F. Chapman in the U.K. We should like from locally produced insects. especially to thank CIBA-GEIGY Ltd., Basel, Swit• zerland, for financial support and the Ministry of Diapause in H. armigera was found to be faculta• Agriculture, Fisheries and Food for Licence No. HH tive, and would occur in cold weather in irrigated 10899/170 to import insects. crops. A possible mechanism for passing the hot dry season and synchronizing emergence with the start of the rainy season was suggested. The sensi• tivity of the prepupae to moderate temperatures (averting diapause) may explain why Balla (1970, References 1973) obtained low proportions of diapause pupae. However, not all pupae entered diapause in any BALLA, A.N. 1970. American bollworm in the Gezira treatment, and so continous breeding on vegeta• and Managil. Pages 281-292 i n Cotton growth in the bles in the dry season in the Sudan no doubt also Gezira environment (eds. W.A. Siddig and L.C. Hughe s ) . o c c u r s . Gezira Research Station Symposium 1969, Wad Medani, S u d a n . The phenology of diapause in H. fletcheri s u g •

gested that this insect is adapted to survive In BALLA, A.N. 1973. Some aspects of the ecology, biol• rainfed conditions, since September to October is ogy and control of American bollworm in the Sudan Ge z • the end of the rainy season in central Sudan. The ira and Managil. Presented at the CIBA-GEIGY recent finding of H. fletcheri as part of the Gezira Conference, February 1973, Gezira Agricultural pest complex verifies Hardwick's (1965) sugges• Research Station, Wad Medani, Sudan.

36 B O W D E N , J . , a n d G I B B S , D . G . 1 9 7 3 . Light t r a p a n d b o l l w o r m ' . P e s t i c i d e s A r t i c l e s a n d N e w s S u m m a r i e s 2 5 : suction trap catches of insects in Northern Gezira, Sud a n 3 1 6 - 3 1 7 . in the season of southward movement of the Intertropical Front. Bulletin of Entomological Research 62: 571 -579 . H A G G I S , M . J . 1 9 7 8 . Distribution of American bollworm eggs in the Sudan Gezira: spatial and temporal change s C A L D W E L L , R.L. 1974. A c o m p a r i s o n of t h e m i g r a t o r y and their relation to weather. Pages 34-67 in Proceedings, strategies of two milkweed bugs, Oncopeltus fasciatus Third Seminar for Cotton Pest Control in the Sudan, CIBA- a n d Lygaeus kalmii. Pages 304-316 in Experimental anal• G E I G Y , B a s e l , S w i t z e r l a n d . y s i s of i n s e c t b e h a v i o r ( e d . L. B u r t o n - B r o w n e ) . Berlin: Springer-Verlag. H A G G I S , M . J . 1 9 8 1 . Spatial and temporal changes in t h e distribution of e g g s of Heliothis armigera ( H u b n e r ) C A L L A H A N , P.S. 1 9 5 8 . B e h a v i o r o f t h e i m a g o o f t h e (Lepidoptera: Noctuidae) on cotton in the Sudan Gezi r a . corn earworm Heliothis zea ( B o d d i e ) . A n n a l s of t h e E n t o • Bulletin of Entomological Research 71:183-193. mological Society of America 51: 271 -283. H A R D W I C K , D . F . 1965. The corn earworm complex. C A L L A H A N , P.S. 1 9 6 2 . Techniques for rearing the corn M e m o i r s o f t h e E n t o m o l o g i c a l S o c i e t y o f C a n a d a 4 0 , e a r w o r m Heliothis zea ( B o d d i e ) . J o u r n a l of E c o n o m i c Ottawa, Canada. 247 pp. Entomology 55: 453-457. H W A N G , G . H . , and H O W , W . W . 1 9 6 6 . S t u d i e s o n t h e C A L L A H A N , P.S., S P A R K S , A . N . , S N O W , J . W . , a n d flight of t h e A r m y w o r m m o t h Leucania separata (Walker). C O P E L A N D , W . W . 1 9 7 2 . Com earworm. Vertical distri• I. Flight duration and wingbeat frequency. Acta Entomo- bution in nocturnal flight. Environmental Entomology 1 : logica Sinica 15: 96-104. (Chinese, with English sum- 4 9 7 - 5 0 3 . mary.) Review of Applied Entomology, Series A 55:88-89.

C O W L A N D , J . W . 1 9 3 5 . American bollworm Heliothis I S E L Y , D . 1 9 3 5 . Relation of hosts to the abundance of obsoleta. P a g e s 1 1 3 - 1 1 8 in Annual Report, 1934-1935, cotton bollworm. University of Arkansas Agricultural Agricultural Research Division, Sudan. Experiment Station Bulletin 320:1-30.

D I N G L E , H . 1965 . The relation between age and flight J O H N S O N , C . G . 1 9 6 9 . Migration and dispersal of activity in the milkweed bug Oncopeltus fasciatus. J o u r • i n s e c t s b y flight. L o n d o n , U K : M e t h u e n . 7 6 3 pp. nal o f E x p e r i m e n t a l B i o l o g y 4 2 : 2 6 9 - 2 8 3 . J O Y C E , R.J.V. 1 9 7 6 . Insect flight in relation to problems D I N G L E , H . 1 9 7 8 . Migration and diapause in tropical, of pest c o n t r o l . P a g e s 1 3 5 - 1 5 5 in I n s e c t flight ( e d . R.C. temperate and island milkweed bugs. Pages 254-275 i n Rainey). Symposia of the Royal Entomological Society o f Evolution of insect migration and diapause (ed. H. Ding l e ) . London 7. Oxford, UK: Blackwell. Berlin: Springer-Verlag. J O Y C E , R.J.V. 1 9 7 8 . Yield response of Gossypium bar- D I N G L E , H . , a n d A R O R A , C . 1 9 7 3 . Experimental stu• badense in the Sudan Gezira to aerial spraying at ULV d i e s of m i g r a t i o n of t h e b u g s of t h e g e n u s Dysdercus. r a t e s w i t h N u v a c r o n 40 . P a g e s 2 2 9 - 2 4 2 in Proceedings, Oecologica 12: 119-140. Third Seminar on Strategy for Cotton Pest Control in t h e S u d a n , C I B A - G E I G Y , B a s e l , S w i t z e r l a n d . G A T E H O U S E , A . G . , a n d H A L L , M . J . R . 1 9 7 6 . T h e effect of isolation on flight and on the pre-ovipositi o n K E H A T , M . , a n d W Y N D H A M , M . 1 9 7 3 . The relation period in unmated Dysdercus superstitiosus. Physiolog i • between food, age and flight in the Rutherglen bug Nysius c a l E n t o m o l o g y 1 : 1 5 - 1 9 . vinitor (Hemiptera: Lygaeidae). Australian Journal of Z o o l o g y 2 1 : 4 2 7 - 4 3 4 . G R O S S , H.R., a n d Y O U N G , J . R . 1 9 7 7 . Comparative development and fecundity of corn earworm reared on K E N N E D Y , J . S . 1 9 6 1 . A turning point in the study of selected wild and cultivated early season hosts commo n insect migration. Nature (London) 189: 785-791. in the Southeastern U.S. Annals of the Entomological S o c i e t y o f A m e r i c a 70: 6 3 - 6 5 . K I S H A B A , A . N . , H E N N E B E R R Y , T . J . , H A N C O C K , P.J., and T O B A , H . H . 1 9 6 7 . Laboratory technique for H A C K E T T , D . S . 1 9 8 0 . B i o l o g y of Helicoverpa armigera studying flight of Cabbage looper moths and the effect o f i n t h e S u d a n G e z i r a . Ph.D. t h e s i s , U n i v e r s i t y o f W a l e s , age, sex, food and tepa on flight characteristics. Jour n a l Cardiff, U.K. o f E c o n o m i c E n t o m o l o g y 6 0 : 3 5 9 - 3 6 6 .

H A C K E T T , D . S . , a n d G A T E H O U S E , A . G . 1 9 7 9 . N e w K O E R W I T Z , F.L., a n d P R U E S S , K.P. 1 9 6 4 . M i g r a t o r y r e c o r d s of Helicoverpa fletcheri Hardwick from the Sudan potential of the Army cutworm. Journal of the Kansas Gezira and observations on diapause in the 'American Entomological Society 37: 234-239.

37 LEPPLA, N.C., HAMILTON, E.W., GUY. R.H., and LEE, F.L. 1979. Circadian rhythms of locomotion in six Noctuid species. Annals of the Entomological Society o f America 72: 209-215.

MORTON. R., TUART, L.D., and WARDHAUGH, K.G. 1 9 8 1 . The analysis and standardisation of light-trap c a t c h e s of Heliothis armiger (Hubner) and H. punctiger Wallengren (Lepidoptera: Noctuidae). Bulletin of En t o m o • logical Research 71; 207-225.

PARSONS, F.S., and MARSHALL, J. 1939. Investiga• tions on the American bollworm. Progress Reports, Experiment Stations, Empire Cotton Growing Corp., S o u t h African Cotton Experiment Station, Barberton, Seaso n 1937-1938:28-35.

RANKIN, M.A., and RIDDIFORD, L.M. 1977. T h e hor• monal control of migratory flight in Oncopeltus fasciatus: The effects of the corpus cardiacum, corpus allatum a n d starvation on migration and reproduction. General an d Comparative Endocrinology 33: 309-321.

ROOME, R.E. 1979. P u p a l d i a p a u s e in Heliothis armigera (Hubner) (Lepidoptera: Noctuidae) in Botswana: its regulation by environmental factors. Bulletin of En t o m o • logical Research 69: 149-160.

SCHAEFER, G.W. 1976. Radar observations on insect flight. Pages 157-197 in Insect flight (ed. R.C. Rainey). Symposia of the Royal Entomological Society of London 7. Oxford, UK: Blackwell.

SHARP, J.L., MCLAUGHIN, J.R., ASHLEY,, T.R., and BENNETT, D.R. 1975. Flight activity of Trichoplusia ni in the laboratory. Annals of the Entomological Society of America 68: 755-758.

TOPPER, C. 1978. The incidence of Heliothis armigera larvae and adults on groundnuts and sorghum and the prediction of oviposition on cotton. Pages 17-33 in P r o • ceedings, Third Seminar on Strategy for Cotton Pest C o n • trol in Sudan. CIBA-GEIGY, Basel, Switzerland.

WILSON, A.G.L., LEWIS, T., and CUNNINGHAM, R . B . 1 9 7 9 . Overwintering and spring emergence of Heli• othis armiger (Hubner) (Lepidoptera: Noctuidae) in the Namoi Valley, New South Wales. Bulletin of Entomolog i • cal Research 69: 97-109.

3 8 The Potential Contribution of Moth Behavior Research to Heliothis Management

P.D. Lingren, A.N. Sparks, and J.R. Raulston*

Abstract

Recently several tools and techniques have been developed for, or adapted to, the study of the nocturnal behavior ot Heliothis spp. As a result, a great deal of information has been collected on the nocturnal behavior of certain species, such as the tobacco budworm, Helio• this virescens (F.). For instance, their diet patterns of emergence, feeding, oviposition, sex pheromone secretion, male searching behavior, pheromone trap response behavior, mating, resting, and, to some extent, their in-field movement have been partially described. Along with other knowledge ot their biology, this information also allows the typing of populations as to their age structure, mating status, and generation dynamics. This paper reviews the status of knowledge relevant to the nocturnal behavior of Heliothis spp, references current methods for obtaining that knowledge, and describes its current uses and some potential ones for the management of H e l i o t h i s spp populations.

The adults of Heliothis spp are primarily active at 1972; Hendricks et al. 1973; Haile et al. 1975; night, and very little is Known about their nocturnal Schaefer 1976; Phillips 1979; Raulston 1979; behavior. This is somewhat surprising when one Sparks 1979; Lingren and Wolf 1982), and the considers that the adult female essentially controls females oviposit on a wide range of host plants the food supply of her progeny by placement of (Brazzel et al. 1953; Hardwick 1965; Neunzig 1969; eggs. The resulting larvae are not highly mobile and Teitz 1972; Martin et al. 1976; Pretorius 1976). This are therefore largely restricted to the food supply promotes, or even ensures, survival of Heliothis selected by the adult female. In contrast, the adults spp individuals over a broad range of environmen• are highly mobile (Hardwick 1965; Callahan et al. tal conditions. The difficulties of protecting crop plants from such polyphagous pests are apparent; however, adequate knowledge of the dynamics of Heliothis spp populations in relation to their various *U.S. Department of Agriculture, Agricultural Research Service; host plants (Adkisson 1971; Knipling 1979) and respectively: Western Cotton Research Laboratory, Phoenix, Ariz; their nocturnal behavior in these plant ecosystems Southern Grain Insects Research Laboratory, Titton, Ga; and Cotton Insects Research Laboratory, Brownsville, Tex, USA. may provide the basis for an attack on the weakest

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings ot the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, AP., India 3 9 links in their population cycles (Lingren 1978; significant damage to crops even under current Lingren et al. 1982; Lingren and Wolf 1982). control procedures? The answer to this question is ln this paper we will review some of the biology of not simple; however, a paramount reason for the Heliothis spp in relation to their nocturnal behavior, current approach is a lack of knowledge of adult which we feel is important to the management of behavior. This information may result in develop• populations. We will deal primarily with adults, but ment of efficient suppression techniques of the nocturnal behavior of larvae is also important and adult life stage, but the literature shows that until the will be discussed. Our discussion will be mostly last decade, little effort has been made to obtain limited to our experience with the tobacco bud- such behavioral information. Of the many reasons w o r m , Heliothis virescens (F.) and the bollworm, for this lack of effort, we consider the following to be Heliothis zea (Boddie). Selected references will be among the more important: (1) general diurnal used to provide historical background and to direct human behavioral patterns; (2) lack of good night the reader to sources of information that are impor• vision in humans; (3) severe restrictions by the tant to an overall understanding of our philosophy. scientific community on the publication of qualita• Much of this presentation will be of a qualitative tive information resulting from our inability to nature and may thus be considered somewhat reduce the variability of biological systems to qua n • speculative. Qualification is, however, a major pre• titative measures; (4) large labor and insect- requisite to quantification, and is thus very impor• density requirements for gathering adequate tant to the understanding of biological organisms information; and (5) profitability of larval control that are by nature highly variable. procedures using pesticides. However, despite these restrictions, a beginning has been made A recent bibliography on the tobacco budworm toward an understanding of the nocturnal behavior and bollworm (Kogan et al. 1978) provides an of the tobacco budworm and bollworm, and, in our excellent reference to past work, and accounts of opinion, this knowledge offers great potential to the biology of the two species from various areas of increase the efficiency of current control technol• their distribution can be found in Quaintance and ogy and for the development of new control Brues (1905); Brazzel et al. (1953); Wilcox et al. procedures. (1956); Hardwick (1965); Lincoln et al. (1967); Neunzig (1969); and Mongrut-Olivares (1971). One outstanding aspect of the biology of these species is that a female of either species can produce over Tools and Techniques for Studying 1000 eggs. However, there is a great deal of varia• Nocturnal Behavior tion in the numbers of eggs produced per female, depending on the individual (Proshold et al. 1982), Several tools are available for studying various the species (Brazzel et al. 1953; Wilcox et al. 1956), aspects of the nocturnal behavior of Heliothis spp, and the larval food source (Lukefahr and Martin such as head lamps, monocular and binocular 1964; Neunzig 1969; Mongrut-Olivares 1971). If we night-viewing devices, pheromone traps, malaise assume that one female per acre (0.4 ha) produces traps, mating tables, actographs, and radar. Sev• 1000 eggs and that half of those eggs produce eral recent papers describe these tools and some larvae that live to even the fourth instar, then the of their uses (Raulston et al. 1975, 1979; Mitchell et economic threshold has been surpassed on a high al. 1976; Schaefer 1976; Lingren et al. 1976, 1979, cash value crop such as lettuce. Five females per 1980, 1982; Sasaki and Ohguchi 1978; Sparks et al. acre could potentially produce enough progeny to 1979a, 1979b; Greenbank et al. 1980; Lingren and surpass the economic threshold on a lower cash Wolf 1982). Obviously, this list of references indi• value crop such as cotton (Adkisson 1964; Ridg- cates that a great deal of work has been done on way 1969). Indeed, economic thresholds may be the nocturnal behavior of certain Heliothis spp, but somewhat misleading, since control procedures their nocturnal behavior as a group is still not well aimed at the larvae seldom result in more than 85% understood. mortality, and the crop sustains considerable dam- Historically, one of the major constraints to col• age even while under a control program that is lection of data on the nocturnal behavior of Helio• considered to be economically sound. this spp has been the lack of use or misuse of Why then have we aimed a majority of our control visible light in the form of head lamps, flashlights, efforts at the larval stage, whose density can be and lanterns. Early workers assumed that little valid 500 to 1000 times that of its parent and can cause information could be gathered on nocturnal behav-

4 0 ior of the species since the insects reacted to the are normally observed about 30 min after initiation wavelengths emitted in white light. Consequently, of the fast flight activity. Secretion of the sex phero - they covered their lights with red filters, which mone by laboratory-reared females (positioned greatly restricted their field of view. Although Helio- near the top of the plants) released in the field this spp do respond to visible light, either in a nega• usually begins about 15 min after the beginning of tive (escape response) or positive (attraction) the fast flight activity of the males. We have manner, many of these responses can De avoided observed very few native females calling in the by first locating the insect with a bright b e a m of light field, except when the population was exposed to and then covering the beam with a red filter or by disruption efforts with their sex pheromone. Even averting the beam so that the insect is located in then the disruption of mating was only temporary, the outer fringes of the beam. Moreover, insects in lasting about a couple of hours. various modes of behavior, such as newly emerged Mating activity in the field generally begins about adults or mating pairs, are unable to escape from 4 hr after sundown and continues for about 4 hr with t h e b e a m of light e v e n if they react to it. Similarly, a majority of the activity taking place between mid• the adults that are deeply involved in a particular night and 0200 hr. Temperature and daylength mode of behavior, such as calling or feeding, may modulate the time that mating takes place. On cool show an initial reaction to the light beam, but they nights and short days, the mating, as well as the will generally continue their original activity within a whole sequence of nocturnal activity, occurs ear• short time even in the presence of the light. There• lier in the evening than on warm nights and long fore, white light is still one of our better tools for days. Tobacco budworm adults dark-adapted in gathering information on many types of nocturnal the laboratory generally start mating about 4 hr insect activity. after being placed in the dark, but they begin their sequence of nocturnal activity in 15 to 30 min. Agee (1969a, 1969b) reports similar activity for the bollworm. Nocturnal Behavior of Tobacco Tobacco budworm (Lingren et al. 1982) and boll- Budworm and Bollworm worm (Callahan 1958) adults emerge at night and it is likely that other species of Heliothis follow a A description of the nocturnal behavior of adult similar pattern. Peak emergence of the tobacco tobacco budworms is given in several recent pap• budworm occurs between 2300 hr and midnight, ers (Lingren et al. 1977a, 1977b, 1978, 1979, 1982; after which they crawl to the top of the plants and Raulston et al. 1975, 1976, 1979, 1980; Sparks et al. remain very docile and relatively inactive for about 1979b; Lingren and Wolf 1982). Initial nocturnal 4 hr. Bollworm e m e r g e n c e also o c c u r s at night, but activity begins about 1 hr after sundown, with a appears to occur earlier. Tobacco budworms do spurt of flight that is generally oriented downwind not mate on the night of e m e r g e n c e , but both sexes (Lingren and Wolf 1982). This activity lasts for are capable of mating the following night. Following about 10 min, and then large numbers of moths of an initial mating, females generally do not mate for both sexes can be observed moving upwind and 2 or 3 days (Raulston et al. 1975); however, males feeding on plant nectaries and other sources of can mate every night, so as a populaton ages an sugar (Lingren et al. 1978). Oviposition activity is excess male mating potential is created. In other heavily interspersed with the feeding activity words, at some period during each generation (Lingren et al. 1979). The major part of feeding and cycle, males are available and searching for mates, oviposition activity occurs within a 3-hr period, but but few females are receptive to mating (Lingren et intermittent feeding and oviposition continues al. 1982). A delay in the initial mating greatly red u • throughout the night, followed by an intense spurt of ces the numbers of eggs produced by females activity about an hour prior to daylight (Lingren et al. (Proshold et al. 1982). A k n o w l e d g e of the emer• 1977a, 1979). An inactive period occurs for about gence patterns is very important to the use of noc• 15 to 30 min after major feeding and oviposition turnal observation techniques in assessing activity subsides. This inactivity has also been population age structure and generation dynamics, observed in laboratory studies on the bollworm as well as adult control with pesticides (Lingren et (Agee 1969a, 1969b). Near the end of the inactive al. 1982; Raulston et al. 1979) period, males begin a fast flight movement oriented An account of the nocturnal behavior of the boll- crosswind (Lingren et al. 1982), and mating pairs worm can be gleaned from laboratory studies (Cal-

41 lahan 1958; A g e e 1969a, 1969b); however, field plants during the night. We do not know if the boll- studies on the nocturnal behavior of this species w o r m or other Heliothis spp exhibit similar behav- are extremely limited, and it was 1962 before an ior, but such behavior is extremely important to the observation of mating in the field was reported timing and placement of materials for larval control. (Phillips and Whitcomb 1962), in which case three The main problem with control of Heliothis spp pairs were observed after 80 nights of observation. larvae is that we know very little about their behav• A primary reason for this lack of information may be ior. Although a limited amount of information has that the researchers were concerned that white been reported on the behavior of larvae of the visible light would disturb the adults, so they used tobacco budworm (Mistric and Smith 1969) and red filters, which restricted their range of view to bollworm (Barber 1941), to our knowledge, the only a few feet. behavior of a Heliothis spp larva has never been Since 1962, we have observed thousands of described from hatch to pupation. Nor have we mating pairs of bollworms in the field and collected seen an account of the behavior of any insect larva some information of their diel patterns of feeding, throughout its larval cycle. This seems deplorable, oviposition, resting, pheromone secretion, since a majority of our chemical control proce• pheromone-trap response activity (Sparks et al. dures have been aimed at larvae, and it is well 1979a), and in-field mating. The only major differ- known that many of their biological activities are of ences observed in the nocturnal behavior of the a circadian nature (Minis and Pittendrigh 1967). bollworm and tobacco budworm have been the Therefore it is highly likely that larvae of Heliothis spp timing, the activities of the bollworm occurring eclose, molt, rest, feed, a n d p u p a t e in rhythmic s o m e w h a t earlier. cycles. Full knowledge of these cycles is extremely Interestingly, bollworm males have been important in effective and efficient use of observed responding to pheromone traps baited population-suppression procedures for the with virgin female tobacco budworms and their species. seven-component synthetic pheromones. Also, male bollworms have been observed mating with tobacco budworm females in nature. We have observed no other mating combinations between Potential Uses of Information on the two species. Indeed, these observations are not Nocturnal Behavior of Heliothis surprising, since the tobacco budworm pheromone contains all four components that constitute the A relatively good account of the present and poten• pheromone of the bollworm (Klun et al. 1979; tial uses of nocturnal behavior information against Sparks et al. 1979a, 1979b). Nevertheless, the mat- Heliothis spp populations is available in two recent ings that we have observed between the two spe• papers (Lingren et al. 1982; Lingren and Wolf cies were not viable. Hardwick (1965) has reported 1982). Therefore, we will deal with this topic in a viable offspring in only one case out of many inter• rather general manner and make an effort to specific crosses between Heliothis spp; however, expand on previous coverage of the subject as well interspecific hybrids have been produced from as point out additional potential uses. crosses between the tobacco budworm and Helio• this subflexa (Guenee) (Laster 1972), and males produced from a backcross between the hybrid Population Age Structure and female and native males produce sterile males and Generation Cycling fertile females. A backcross of this hybrid is cur• rently being tested as a population-suppression The sequence of nocturnal activities described for procedure for tobacco budworm on the island of St. tobacco budworm and bollworm indicates that Croix, U.S. Virgin Islands. adults (newly emerged, calling females, mating The larvae of the tobacco budworm leave the pairs, and resting singles) and larvae (molting) cotton fruit during the night and move to the top of occupy the terminal portions of plants during spe• the plants to molt (Lingren and Wolf 1982). After cific periods of the night. In natural populations molting, they eat their cast skins, a n d appear to most of these forms exhibit no major movement remain on the tops of the plants until their exoske- activity and are therefore rather easily observable letons are cured. Also, Neunzig (1969) reported at night. This allows collection of adults and typing that tobacco budworm larvae moved from tobacco of the population in terms of its generation age

42 structure (Raulston et al. 1979) and mating poten• adults for species comparisons. Density assess• tial (Lingren et al. 1982). Barber (1937) reported ments can be obtained from relative captures per that four to six generations of the tobacco budworm unit area or time period.The capture of native males occurred annually in eastern Georgia, and that in live traps (Raulston et al. 1980) also allows mark- these generations were distinct and separated by release and recapture of native insects. Compari• periods in which larvae were not found. Our expe• sons of the capture-recapture ratios of native rience from coast to coast throughout the southern males, along with comparative mating interactions USA suggests similar population trends. This sug• of the marked and unmarked males, appear to offer gests that populations emerge and age in a rather a relatively good means for density determination predictable manner. We have shown that night- (unpublished data). observation techniques can be used to type these populations according to their generation age structure (Lingren et al. 1982). The adults of a given Population Forecasting generation do emerge rather rapidly, mate, and age in a potentially predictable manner (Raulston et al. Knowledge of the population age structure and 1979). The age structure of the overall population generation dynamics obtained by night- presents different levels of pressure on control observation techniques, along with other informa• p r o c e d u r e s (Lingren et al. 1982); therefore, the tion on the developmental and mating biology of the density and the age structure of a population tobacco budworm, should allow us to forecast the should determine the type of suppression to be time of occurrence of future generations. We have used, as well as the timing, dosage, and numbers observed that temperatures generally are optimum (parasites, predators, and sterile releases), of a for development during the primary fruiting period specific procedure. of the plants and cycles occur al about 28-day According to Barber (1937), generations of the intervals. We have been able to use the projection bollworm tend to overlap. This may be due in part to in our research and many of the pest-control advi• a developmental period that is 2 to 3 days longer sors in the western United States commonly use than that of the tobacco budworm. However, our verbal projections for timing of pesticide appli• unpublished data that we have collected overtime cations. Moreover, the senior author feels, on the indicate that a majority of a generation emerges basis of several field trials, that the potential density and mates over a 9-day period. Therefore, their of future generations (at least the next generation) generation cycles on cotton appear to be some• on cotton in the western USA can be predicted with what similar to that of the t o b a c c o b u d w o r m during relatively good accuracy from nocturnal studies. the major fruiting period of the crop. Alternative host plants and their relative maturity would influ• ence these cycles, which would therefore probably Adult and Larval Suppression from be somewhat different for each major ecosystem. Nocturnal Applications of Insecticides Immature forms of some Heliothis spp are much more difficult to control with pesticides than others; Good kill of adult tobacco budworms has been therefore, immediate knowledge of the species accomplished through nighttime applications of composition within an area is necessary for effi• insecticides timed to take advantage of an emerg• cient application of an effective control procedure ing population and adult activities on the terminal and for accurate evaluation of the effect of control portion of the plant (Lingren et al. 1982). Also, procedures such as sex pheromones. This is espe• observations indicate that larvae of the tobacco cially true when egg and larval counts are used as a budworm move to the top of the plant to molt measure of efficacy. However, the immature forms (Lingren and Wolf 1982), thus becoming exposed of most Heliothis spp are difficult to separate, while to direct contact from sprays applied at night. A the adult forms are sometimes distinctly different more thorough knowledge of this larval behavior (for example, bollworm vs. tobacco budworm). could be very advantageous to the more efficient Knowledge of the nocturnal behavior of adults use of microbials (Bell and Kanavel 1978) formu• along with night observations offer an immediate lated with feeding adjuvants, especially when the solution to this problem and relative density crop canopy has overlapped the rows. Under this assessments can be obtained. In other words, an situation, nighttime control applications should be observer can go into the field at night and collect more effective than daytime applications. Indeed,

43 nighttime applications of insecticides for larval a n d Chemical Communication adult control have b e c o m e m u c h m o r e prevalent in the s o u t h w e s t e r n U S A during the past f e w years. It is interesting to note that molecular vibrations p r o d u c e f r e q u e n c i e s that c o r r e s p o n d to w a v e - lengths in the far infrared (Wright 1980) a n d that Nocturnal Predation optically inactive isomers will exhibit circular di- c h r o i s m w h e n p l a c e d in an optically active solvent W h i t c o m b a n d Bell (1964) have o b s e r v e d several (Wright 1977). This activity is also observable in the s p e c i e s of nocturnal predators feeding on o n e or far infrared. Wright (1954, 1977, 1980) suggests m o r e of the life stages of the bollworm a n d t o b a c c o that these p h e n o m e n a are very important to odor b u d w o r m . In our nocturnal studies we have stimulus-receptor interaction, and are probably the o b s e r v e d that earwigs, assassin bugs, a n d spiders m e a n s by w h i c h insects r e s p o n d to various stimuli. are the foremost arthropod predators of Heliothis C a l l a h a n (1965a) also a d v o c a t e s a far infrared spp. T h e earwigs appear to be t h e most important e l e c t r o m a g n e t i c theory of c o m m u n i c a t i o n a n d of this group. However, in o n e test we released s e n s i n g by the c o r n e a r w o r m (Callahan 1965b, 2 4 0 0 t o b a c c o b u d w o r m adults in cotton a n d 1 7 % of 1969) a n d other night-flying moths (Callahan a n d the adults w e r e c a p t u r e d on the first night by the L e e 1974). T h e c o n c e p t s of these two scientists g r e e n lynx spider, Peucatia viridins (Hentz). On m a y lead to a major a d v a n c e m e n t in an under• n u m e r o u s o c c a s i o n s , t h e senior author has standing of insect c o m m u n i c a t i o n s . If so, a n d if o b s e r v e d m o t h s hovering a r o u n d several species moths do locate their host plants through far of spiders as if they w e r e attracted to t h e m . T h i s infrared emissions, t h e n major n e w a p p r o a c h e s to p h e n o m e n o n generally o c c u r s during the sexually insect suppression are on the horizon. A better active period of the moths. Collections of moths understanding of the nocturnal behavior of moths c a p t u r e d by t h e s e spiders s h o w that s o m e species a n d their flight activities will play a major role in the c a p t u r e primarily males, while others c a p t u r e prim• d e v e l o p m e n t o f t h e s e n e w s u p p r e s s i o n arily females. Eberhard (1977) has s h o w n that the procedures. bolas spiders use c h e m i c a l mimicry to attract a n d c a p t u r e adult m a l e fall a r m y w o r m s . Therefore, an intensive investigation into the m e a n s that certain T h e F u t u r e spiders use for obtaining their prey c o u l d lead to the identification of n e w attractants or m o r e effective We feel that the information d e v e l o p e d on the noc• use of these predators as biological control agents. turnal behavior of Heliothis spp c a n potentially be u s e d for m o r e rapid or better technological a d v a n c e m e n t in: (1) in-field speciation, (2) i m p a c t of most types of control programs, (3) population Evaluation of Population-Suppression density a s s e s s m e n t s , (4) population a g e structure Programs Involving Mating determinations, (5) population e m e r g e n c e fore• casting, (6) trap design a n d efficiency, (7) noctur• In t h e past, most investigations a i m e d at population n a l p r e d a t i o n , ( 8 ) p o p u l a t i o n m o v e m e n t s u p p r e s s i o n t h r o u g h mating interaction or mating determination, (9) target selection in t e r m s of life s u p p r e s s i o n w e r e evaluated by indirect methods, stage, (10) identification of possible n e w attrac• s u c h as p h e r o m o n e traps, light traps, or s u b s e • tants, (11) m o r e effective a n d efficient use of cur• quent p r o d u c t i o n of i m m a t u r e forms. U s e of s u c h rent control procedures, a n d (12) design of n e w evaluation p r o c e d u r e s is rather tenuous, unless a n d m o r e effective control p r o c e d u r e s . o n e k n o w s their relationship to the behavior being T h e d e g r e e a n d s p e e d of s u c h a d v a n c e s will altered. N o c t u r n a l observation t e c h n i q u e s c a n be d e p e n d a great deal on the n u m b e r of observers, u s e d to directly m e a s u r e t h e impact on mating or their observational ability, a n d their capacity for m a t i n g interaction that is o c c u r r i n g in the field communicating primarily qualitative information. (Raulston et al. 1975, 1976; Lingren et al. 1979, A d e q u a t e observations of the nocturnal behavior of 1982). Establishment of relationships b e t w e e n Heliothis s p p — o r , as far as that goes, any direct a n d indirect methods of evaluation of mating s p e c i e s — a r e labor-intensive a n d d e p e n d e n t o n d e p r e s s a n t s or interactions is a prerequisite to the density of the target. Therefore, countries or proper program evaluation. organizations with a d e q u a t e supplies of relatively

44 cheap trained technical personnel can contribute infrared (FIR) electromagnetic theory of communicati o n substantially to future advancements in the control and sensing in moths and its relationship to the limiting or Heliothis spp. biosphere of the corn earworm. Annals of the Entomo l o g i • cal Society of America 58:727-745.

CALLAHAN, P.S. 1965b. Far infrared emission and detection by night flying moths. Nature 207:1172-11 7 3 .

References CALLAHAN, P.S. 1969. The exoskeleton of the corn earworm moth Heliothis zea Lepidoptera: Noctuidae with ADKISSON, P.L. 1971. Weak links in the population special reference to the sensilla as polytubular diel e c t r ic dynamics and diapause of Heliothis zea ( B o d d i e ) w h i c h arrays. Pages 5-105 in University of Georgia Agricultural might be exploited by the sterile-insect release te c h n i q u e . Experiment Station Research Bulletin 54,Tifton, Ga, U S A . Pages 355-364 in Sterility principle for insect control or eradication. International Atomic Energy Agency, Vie n n a , CALLAHAN, P.S., and LEE, F. 1974. A v e c t o r a n a l y s i s Austria. of the infrared emission of night flying moths, wit h a d i s • cussion of the system as a directional homing device . ADKISSON, P.L., HANNA, R.L., and BAILEY, C.F. Annals of the Entomological Society of America 67:341 - 1964. Estimates of the numbers of Heliothis larvae per 355. acre in cotton and their relation to the fruiting cy c l e a n d yield of the host. Journal of Economic Entomology CALLAHAN, P.S., SPARKS, A.N., SNOW, J.W., and 5 7 : 6 5 7 - 6 6 3 COPELAND, W.W. 1972. Corn earworm moth: vertical distribution in nocturnal flight. Environmental Entom o l o g y AGEE, H.R. 1969a. Response of flying bollworm moths 1:497-503. and other typmanate moths to pulsed ultrasound. Ann a l s of the Entomological Society of America 62:801 -807. EBERHARD, W.G. 1977. Aggressive chemical mimicry by a bolas spider. Science 198:1173-1175. AGEE, H.R. 1969b. Mating behavior of bollworm moths. Annals of the Entomological Society of America 62:11 2 0 - GREEN BANK, D.O., SCHAEFER, G.W., and RAINEY, 1 1 2 2 . R.C., 1980. Spruce budworm (Lepidoptera: Tortricidae) moth flight and dispersal: new understanding from c a n • BARBER, G.W. 1937. Seasonal availability of food opy observations, radar, and aircraft. Memoirs of t h e plants of two species of Heliothis in eastern Georgia. Entomological Society of Canada 110, Ottawa, Canada. Journal of Economic Entomology 30:150-158. 49 pp.

BARBER, G.W. 1941. Observations on the egg and HAILE, D.G., SNOW, J.W., and YOUNG. J.R. newly hatched larva of the corn ear worm on corn silk. 1975. Movement by adult Heliothis released on St. Croix Journal of Economic Entomology 34:451 -456. to other islands Environmental Entomology 4:225-226.

BELL, M.R., and KANAVEL, R.F. 1978. Tobacco bud- HARDWICK, D.F. 1965. The corn earworm complex. worm: development of a spray adjuvant to increase e f f e c • Memoirs of the Entomological Society of Canada 40, tiveness of a nuclear polyhedrosis virus. Journal of Ottawa, Canada. 247 pp. Economic Entomology 71:350-352. HENDRICKS, D.E., GRAHAM, H.M.. and RAULSTON, BRAZZEL, J.R., NEWSOM, L.D., ROUSSEL, J.S., J.R. 1973. Dispersal of sterile tobacco budworms from LINCOLN. C., WILLIAMS, F.J., and BARNER, G. release points in northeastern Mexico and southern 1953. Bollworm and tobacco budworm as cotton pests in Texas. Environmental Entomology 2:1085-1088. Louisiana and Arkansas. Louisiana Agricultural Exper i • ment Station Technical Bulletin 482, Baton Rouge, Lo u i s i • JOYCE, R.J.V. 1981. The control of migrant pests. ana, USA. 47pp. Pages 209-229 in Animal migration. Society for Experi• mental Biology seminar series 13. Cambridge, UK: Cam• CALLAHAN, P.S. 1958. Behavior of the imago of the bridge University Press. corn earworm, Heliothis zea (Boddie), with special refer• ence to emergence and reproduction. Annals of the E n t o • KLUN, J.A., PLIMMER, J.R., BIERL-LEONHARDT, mological Society of America 51:271 -283. B.A., SPARKS, A.N., and CHAPMAN, O.L. 1979. Trace chemicals: the essence of sexual communi• CALLAHAN, P.S. 1965a. Intermediate and far infrared cation systems in Heliothis species. Science 204:1328- sensing of nocturnal insects. Part I. Evidences for far 1 3 3 0 .

4 5 KNIPLING, E.F. 1979. The basic principles of insect LINGREN, P.D. RAULSTON, J.R., SPARKS, A.N., and population suppression and management. USDA Agricul • WOLF, W.W. 1982. Insect monitoring technology for tural Handbook 512, Washington, DC, USA. 659 pp. evaluation of suppression via pheromone systems. Ch a p • ter 6 in Insect suppression using controlled release KOQAN, J., SELL, D.K., STINNER, R.E., BRADLEY, pheromone systems, Volume I, eds. G. Zinerg, A.F. K y d o - J.R., Jr., and KOGAN, M. 1978. The literature of nieus, and M. Beroza. Boca Raton, Florida: CRC Press. arthropods associated with soybeans: V. A bibliograp h y of Heliothis zea (Boddie) and H. virescens (F.) (Lepidoptera: LUKEFAHR. M.J., and MARTIN, D.F. 1964. T h e Noctuidae). INTSOY Series 17. Champaign-Urbana, III., effects of various larval and adult diets on the fecun d i t y USA: International Agricultural Publications. 242 pp. and longevity of the bollworm, tobacco budworm, and cotton leafworm. Journal of Economic Entomology LASTER, M.L. 1972. Interspecific hybridization of H e l i o - 57:233-235. this virescens a n d H. subflexa. Environmental Entomol- MARTIN, P.B., LINGREN, P.D., and GREENE, G.L. o g y 1 : 6 8 2 - 6 8 7 . 1 9 7 6 . Relative abundance and host preferences of cab• bage looper, soybean looper, tobacco budworm, and c o r n LINCOLN, C. et al. 1967. The bollworm-tobacco bud- earworm on crops grown in northern Florida. Environme n • worm problem in Arkansas and Louisiana. University of tal E n t o m o l o g y 5 : 8 7 8 - 8 8 2 . Arkansas Agricultural Experiment Station Bulletin 720 , Fayetteville, Ark, USA. 66 pp. MINIS, D.H., and PITTENDRIGH, C.S. 1967. C i r c a - dian oscillation controlling hatching: its ontogeny d u r i n g LINGREN, P.D. 1978. Tobacco budworm nocturnal embryogenesis of a moth. Science 159:534-536. behavior—an aid in pest management. Pages C1-3 in Proceedings, Sixth Desert Cotton Insects Symposium, University of California Cooperative Extension Servi c e , El MISTRIC.W.J., Jr., andSMITH, F.D. 1969. Behavior of Centra, Calif, USA. 42 pp. tobacco budworm larvae on flue-cured tobacco and pos • sibilities of improving the effectiveness of insectic i d a l

LINGREN, P.D., and WOLF, W.W. 1982. N o c t u r n a l treatment applied mechanically for control. Journal ot activity of the tobacco budworm and other insects. Pa g e s E c o n o m i c E n t o m o l o g y 6 2 : 1 6 - 2 1 . 2 0 5 - 2 2 2 in The role of biometeorology in integrated pest management, eds. J.L. Hartfield and I.J.Thomason. N e w MITCHELL, E.R., BAUMHOVER, A.H., and JACOB- York, NY, USA:Academic Press. 500 pp. (In press). SON, M. 1976. Reduction of mating potential of male Heliothis s p p a n d Spodoptera frugiperda in field plots treated with disruptants. Environmental Entomology LINGREN, P.D., GREENE, G.L., DAVIS, D.R., BAUM- 5 : 4 8 4 - 4 8 6 . HOVER, A.H., and HENNEBERRY, T.J. 1977a. N o c • turnal behavior of four lepidopteran pests that attac k MONGRUT-OLIVARES, C.A. 1971. Temperature, tobacco and other crops. Annals of the Entomological humidity, and light effects on the reproductive potential of Society of America 70:161-167. Heliothis zea (Boddie) adults in the laboratory. Ph. D. dissertation, University of California, Riverside, Calif, USA. LINGREN, P.D., RAULSTON, J.R., andSPARKS, A.N. 1 8 6 pp. 1977b. Interception of native male tobacco budworm by barriers of released laboratory-reared sterile femal e s . NEUNZIG, H.H. 1969. The biology of the tobacco bud- Environmental Entomology 6:217-221. worm and the corn earworm in North Carolina. North Carolina Agricultural Experiment Station Technical Bu l - LINGREN, P.D., SPARKS, A.N., RAULSTON, J.R., letin 196, Raleigh, NC, USA. 76 pp. a n d W O L F , W . W . 1978. Applications for nocturnal stu• dies of insects. Bulletin of the Entomological Societ y of PHILLIPS. J.R. 1979. Migration of the bollworm, Helio• America 24:206-212. this zea (Boddie). Pages 409-411 in Movement of highly mobile insects: Concepts and methodology in research, LINGREN, P.D., RAULSTON, J.R., SPARKS, A.N., eds. R.L. Rabb and G.G. Kennedy. Raleigh, NC, USA: and PROSHOLD, F.I. 1979. Tobacco budworm. noctur• University Graphics. 456 pp. nal behavior of laboratory-reared irradiated and nat i v e adults in the field. USDA/SEA, Oakland, Calif, USA. ARR- PHILLIPS, J.R., and WHITCOMB, W.H. 1962. Field W - 5 . 1 7 p p . behavior of the adult bollworm, Heliothis zea ( B o d d i e ) . Journal of the Kansas Entomological Society 35:242-246. LINGREN, P.D., BURTON, J., SHELTON, W., and RAULSTON, J.R. 1980. Night vision goggles: for design, PRETORIUS, L.M. 1976. L a b o r a t o r y s t u d i e s o n t h e evaluation, and comparative efficiency determination of a developmental and reproductive performance of Helio• pheromone trap for capturing live adult male pink bo l l - this armigera (Hubn) on various food plants. Journal of the worms. Journal of Economic Entomology 73:622-630. Entomological Society of South Africa 39:337-343.

4 6 PROSHOLD, F.I. KORPENKA, C.P., and GRAHAM, SPARKS, A.N., CARPENTER, J.E., KLUN, J.A., and C . K . 1 9 8 2 . Egg production and oviposition in the tobacco MULLINIX, B.G. 1979a. Field responses of male Helio- budworm. Annals of the Entomological Society of Amer• this zea (Boddie) to pheromonal stimuli and trap design. ica. (In press.) Journal of the Georgia Entomological Society 14: 318- 3 2 5 . QUAINTANCE, A.L., and BRUES, C.T. 1905. T h e c o t • ton bollworm. USDA Bureau of Entomology Bulletin 50, SPARKS, A.N., RAULSTON, J.R., LINGREN, P.D., Washington, DC, USA. 155 pp. CARPENTER, J.E., KLUN, J.A., and MULLINIX, B.G. 1979b. Field responses of male Heliothis virescens to RAULSTON, J.R. 1979. Heliothis virescens migration. pheromonal stimuli and traps. Bulletin of the Entomol o g i • P a g e s 4 1 2 - 4 1 9 in Movement of highly mobile insects: cal Society of America 25: 268-274. Concepts and methodology in research, eds. R.L. Rabb and G.G. Kennedy. Raleigh, NC, USA: University Gra• TEITZ, H.M. 1972. An index to the described life histo• phics, 456 pp. ries, early stages, and host of the macro-lepidopter a of the continental United States and Canada. A.C.AIlyn, RAULSTON, J.R., SNOW, J.W., GRAHAM, H.M., and Allyn Museum of Entomology, Sarasota Fla, USA. 1041 LINGREN, P.D. 1975. Tobacco budworm: Effect of prior pp. mating and sperm content on mating behavior of femal e s . Annals of the Entomological Society of America 68:701 - WHITCOMB, W.H., and BELL, K. 1964. Predaceous 704. insects, spiders, and mites in Arkansas cotton fields. Arkansas Agricultural Experiment Station Bulletin 690 , RAULSTON, J.R., GRAHAM, H.M., LINGREN, P.D., Fayetteville, Ark, USA. 83 pp. and S N O W , J . W . 1 9 7 6 . Mating interaction of native and laboratory-reared tobacco budworms released in the WILCOX, J., HOWLAND, A.F., and CAMPBELL, R.E. field. Environmental Entomology 5:195-198. 1 9 5 6 . Investigations of the tomato fruitworm, its seasonal history and methods of control. USDA Technical Bulletin RAULSTON, J.R., LINGREN, P.D., SPARKS, A.N., 1147. Washington, DC, USA. 47 pp. and MARTIN, D.F. 1979. Mating interaction between native tobacco budworms and released backcross WRIGHT, R.H. 1954. Odor and chemical constitution. adults. Environmental Entomology 8:349-353. Nature 173:831.

RAULSTON, J.R., SPARKS, A.N., and LINGREN, P.D. WRIGHT, R.H. 1977. Odor and molecular vibration: 1980. Design and comparative efficiency of a wind- optical isomers. Chemical Senses and Flavor 3:35-37. oriented trap for capturing live Heliothis spp. J o u r n a l of Economic Entomology 73:586-589. WRIGHT, R.H. 1980. Odor and molecular vibration. P a g e s 1 2 3 - 1 4 1 in Odor quality and chemical structure, RIDGWAY, R.L. 1969. Control of the bollworm and eds. H.R. Moskowitz and C.B. Warren. American Chemi• tobacco budworm through conservation and augmenta• cal S o c i e t y S y m p o s i u m series 1 4 8 . tion of predaceous insects. Pages 127-144 in P r o c e e d • ings, Tall Timbers Conference on Ecological Animal Control by Habitat Management, Tallahassee, Fla, USA. 2 4 4 pp.

N o t e : This paper reports tne results of research only. M e n t i o n o f SASAKI, M., and OHGUCHI, Y. 1978. F e m a l e - a pesticide does not constitute recommendation for u s e b y t h e searching flight rhythm of the male cucumber looper, USDA, nor does it imply registration under FIFRA as a m e n d e d . Anadenidia peponis (Lepidoptera: Noctuidae). Bulletin of Mention of a commercial product does not constitute an endorse• the Faculty of Agriculture, Tamagamo University 18:8- 1 5 . ment of the product by the USDA.

SCHAEFER, G.W. 1976. Radar observations of insect flight. Pages 157-197 in Insect flight, ed. R.G. Rainey. London, UK: Blackwell.

SPARKS, A.N. 1979. An introduction to the status, cur• rent knowledge, and research on movement of selecte d Lepidoptera in southeastern United States. Pages 382 - 3 8 5 i n Movement of highly mobile insects: Concepts and methodology in research, eds. R.L. Rabb and G.G. Kennedy. Raleigh, NC, USA: University Graphics. 456 pp.

4 7 Discussion — Session 1

Dr. Jayaraj explained that his laboratory studies strong winds can affect moth behavior, it is sus- were conducted mainly to determine the suitablity pected that the behavioral mode of the insect at of different species of host plants for the develop • any time will markedly influence its flight activity in ment and reproduction of H. armigera. He a g r e e d relation to the wind. The Heliothis spp moths are that such studies may not reflect the actual suitabil• known to be strong fliers, and good responses of ity of the crops in the field. Further field studies males to virgin females have been observed in would be needed to determine the key mortality winds in excess of 35 mph (56 kmph). factors that would operate on pest populations. The seven-component synthetic pheromone of Dr. Jayaraj was asked whether there are genetic H.virescens has been shown to be much more differences between geographical populations in attractive to males than were virgin females in traps their tendency to enter diapause or whether dia• in field tests in three major climatic zones. How• pause was purely a function of the environment. He ever, the synthetic formulation began to break replied that he had no knowledge of any work on down after about 2 hours, after which male behav• such genetic differences. ioral patterns similar to those induced by the two Dr. Hackett, answering a question on the long major components were noticed. These two com• flights of mated females in his tests, agreed that this ponents are highly attractive, but the males stop may have been due to the absence of host odor. before they reach the point source. The alcohol However, in the USA, mated females have been appears to be the component that separates mat- caught on a TV tower at a height of more than 300 ings between H. zea a n d H. virescens. m, from a population that was thought to be migrat• Dr. Lingren knew of no studies concerning the ing, so the mated females observed in Dr. Hackett's conditioning effect of larval food upon mating tests could well have been behaving naturally. behavior, except that larval diet has been shown to When asked whether there was any indication affect reproductive maturity and mating aggres• that the previous larval history had affected the siveness. The larger welt-fed insects are not flight behavior of the moths, Dr. Hackett said that always the most aggressive. He was unable to offer there was. Moths tested in 1977 were fed an artifi• a good speculative answer to the question why H. cial diet; these did not fly much and oviposited armigera has recently become a major pest on heavily on the fourth day. This was in sharp con• cotton in India. However, he pointed to the similar trast to the moths studied in 1978, which were from adaptation of H. virescens, which has developed as a field crop of sorghum. a major pest of cotton in the USA over the last three Dr. Lingren said that one of the benefits resulting decades. Possible reasons for H. armigera a d a p t a • from nocturnal observations of Heliothis m o th tion to cotton may be changes in varieties, cropping behavior was the more efficient insecticide spray• systems, and cropping practices. There may ing at night. Such spraying is now common practice also have been a mutation in the species. in the western USA, and many operators are spray• ing at specific times of the night to take advantag e of particular behavioral traits, which have been determined by nocturnal observation of the pests. Dr. Lingren confirmed that he regarded release- recapture methods as useful and reasonably effi• cient in studies of Heliothis moths. Studies of moth flight have indicated both short and migratory flight. In newly emerging populations it was observed that the majority of moths left the emergence area dur• ing the early evening and early morning. Night- vision goggles, radar, and radio have been used to observe the flight of Heliothis moths from near the crop canopy to several meters above. Although

4 8 Session 2

Surveillance, Forecasting, and Modeling of Heliothis Populations

Chairman: R.J.V. Joyce Rapporteurs: C.S. Pawar Cochairman: Zile Singh H.C. Sharma

Modeling and Forecasting Heliothis Populations in the USA

A.W. Hartstack*

Abstract

Heliothis spp modeling in the USA has made considerable progress in the past decade; however, there are still many unanswered questions and unknowns in the population dynamics of both species of economic importance. The MOTHZV model, developed in Texas, has been used successfully in the field by the state's Agricultural Extension Service for 6 years. The model was used to predict the timing of oviposition one to two generations ahead; this infor• mation was used by pest managers to time scouting programs, irrigation applications, and insecticide treatments. The MOTHZV model lacks many of the physiological process algo• rithms necessary to predict the number of insects; therefore its predictions are limited to timing only. The paper also reviews other models used to evaluate management strategies tor the pest and identifies some of the areas in which research is needed for building more sophisticated models.

There have been dramatic changes in the control rapid fruiting characteristics, complemented by of cotton insect pests during the last 10 to 15 years, efficient use of fertilizer and water, judicious us e of brought about by insect resistance to pesticides, insecticides, and maximum reliance on naturally changes in government programs, and reductions occurring insect-control factors. in potential profits. Recently, the increasing cost of An important realization in the search for alterna• energy and concern over environmental quality tives was that no single method of control can be have accentuated the need for alternative expected to provide an acceptable solution to all approaches to cotton-pest control. Several new insect problems. The entire cotton-production sys• production systems have been proposed and tem must be examined to decide what techniques tested, based on cotton varieties with early, more are likely to be feasible and practical for a given pest (Knipling 1979). In most cases, more detailed knowledge of the ecology and behavior of the *U.S. Department of Agriculture, Agricultural Research Service, insect is required. The new discipline of integrated Pest Control Equipment and Methods Research Unit, College Station, Tex, USA. pest management has been built on this philosophy

A generalized f r a m e w o r k for insect population The Systems Approach d y n a m i c s as a function of t e m p e r a t u r e w a s d e v e • loped by W a t s o n (1973). This m o d e l has been used T h e integrated pest m a n a g e m e n t a p p r o a c h c a n b e by entomologists for studying t h e d e v e l o p m e n t rate e n h a n c e d b y t h e u s e o f s y s t e m s analysis a n d c o m • a n d population d y n a m i c s of m a n y insects, includ• puter m o d e l s . S y s t e m s m o d e l i n g has e m e r g e d ing Heliothis spp, pink bollworm, a n d Lygus. f r o m m a n ' s n e e d t o study a n d control larger a n d Stinner et al. (1974) d e s c r i b e d a Heliothis m o d e l m o r e c o m p l e x systems. T h e N A S A m o o n explora• for North Carolina conditions. T h e m o d e l included tion p r o g r a m is a p r i m e e x a m p l e of t h e s y s t e m s a spatial grid of fields a n d c r o p types. E a c h c r o p a p p r o a c h , w h e r e multidisciplinary t e a m s with s p e • w a s m o d e l e d on a field basis, using a m e a s u r e of cialized k n o w l e d g e w o r k e d together with t h e aid of t h e a t t r a c t a n c e of the c r o p for Heliothis. W h i l e no s o p h i s t i c a t e d c o m p u t e r s a n d e q u i p m e n t t o solve yield prediction w a s possible, this a p p r o a c h c o m p l e x p r o b l e m s (Witz 1973). D e M i c h e l e a n d a l l o w e d study of the m o v e m e n t of t h e insect p o p u • Bottrell (1976) d i s c u s s in c o n s i d e r a b l e detail the lation; however, the use of this m o d e l w a s limited to s y s t e m s a p p r o a c h to cotton-pest m a n a g e m e n t , the a r e a of N o r t h Carolina w h e r e it w a s developed. stating that this a p p r o a c h is especially useful in As part of a multidisciplinary effort at Mississippi unifying a n d guiding r e s e a r c h a n d in u n d e r s t a n d • State University, B r o w n et al. (1979) a n d J o n e s et ing interactions in the s y s t e m a n d the c o n s e q u e n • al. (1980) have d e v e l o p e d a m o d e l of the cotton c e s of the control tactics applied. c r o p a n d its major pests, the boll weevil a n d Helio• T h e s y s t e m s o r modeling a p p r o a c h usually b e g • this spp. T h e m o d e l brings together previous work ins wit h s i m p l e mental m o d e l s (Witz 1973). " W a t c h on t h e cotton c r o p ( M c K i n i o n et al. 1975), t h e boll out for the July 4 t h bollworm egglay." "Full m o o n weevil (Jones et al. 1977), a n d Heliothis (Hartstack o c c u r s on J u l y 10, so there will be large Heliothis et al. 1976a), a n d is being used to improve pest- s p p e g g l a ys about 2 to 4 days later." " T h o s e m a n a g e m e n t strategies, s u c h as timing of insecti• s u m m e r s h o w e r s will really bring on the boll w e e • c i d e applications, variable e c o n o m i c threshold vil." Every p e r s o n formulates s u c h simple models, levels of pests, a n d various pest-control strategies, b a s e d o n e x p e r i e n c e . including boll weevil eradication. W h e n t h e s e mental models or images are trans• A c o n s i d e r a b l e a m o u n t of Heliothis m o d e l i n g f o r m e d to a flowchart, a set of equations, or a has b e e n d o n e in Arizona (Butler a n d Hamilton c o m p u t e r pro g ra m , they t h e n b e c o m e a tangible 1976), mostly b a s e d on laboratory studies of insect m o d e l that c a n b e c o m m u n i c a t e d t o a n d u s e d b y d e v e l o p m e n t at various t e m p e r a t u r e s (Butler 1976; other people. S u c h m o d e l s m a y t h e n b e c o m b i n e d Butler et al. 1979). T h e models use an algorithm into m o r e c o m p l e x m o d e l s through the use of the d e s c r i b e d by Stinner et al. (1974) on a d e g r e e - d a y c o m p u t e r a n d s y s t e m s analysis t e c h n i q u e s (Witz c o n c e p t for d e v e l o p m e n t d u e to temperature. 1973). Light traps h a v e been u s e d for m a n y years to M o d e l s m a y be c o n s t r u c t e d at various levels of monitor Heliothis m o t h populations. Hartstack et al. detail. T h e level u s e d in a given situation must be (1973) d e v e l o p e d a m o d e l for estimating the d e t e r m i n e d f r o m the intended p u r p o s e of the m o d e l n u m b e r of moths per h e c t a r e from t h e s e light-trap as well as the current k n o w l e d g e available for a c a t c h e s , to evaluate t h e possible u s e of light traps g i v e n s y s t em . T h e possible levels of detail estab• for controlling Heliothis spp. In the last few years, lish a hierarchy of k n o w l e d g e on a g i v e n subject. p h e r o m o n e traps (Hartstack et al. 1979) h a v e An a n i m a l or plant, for example, may be subdivided r e p l a c e d light traps as m o t h - m o n i t o r i n g devices. into t h e b a s i c physiologic p r o c e s s e s , w h i c h in turn M o d e l s are also b e i n g d e v e l o p e d (Hartstack et al. are c o m p o s e d of various o r g a n s a n d c o m p o n e n t s . 1976b; Hartstack a n d Witz 1981) to sort out t h e E a c h o r g a n m a y be studied f r o m the cellular level, various factors affecting p h e r o m o n e trap c a t c h e s . t h e b i o c h e m i c a l level, a n d possibly d o w n t o t h e An important event in the population d y n a m i c s of m o l e c u l a r a n d a t o m i c levels. Detailed models at Heliothis s p p is diapause. Recently a n u m b e r of o n e level c a n often b e simplified a n d m a d e useful m o d e l s d e s c r i b i n g t h e e m e r g e n c e of diap aus in g for application at a higher level w h e r e less p r e c i • p u p a e in t h e spring have been reported ( L o g a n et sion is required. al. 1979; Potter et al. 1 9 8 1 ; Wilson et al. 1979). A

52 major effort is under w a y at C o l l e g e Station, T e x a s , preoviposition adults, a n d ovipositing adults for to construct a diapause e m e r g e n c e m o d e l that c a n e a c h day of the simulation. E a c h stage of the insect be used in a study of early spring migration of was a d v a n c e d one calendar day at a time with a Heliothis into T e x a s from M e x i c o (Hartstack et al. degree-day concept, so that daily mortalities ( n a t u • 1982a, 1982b; Lopez et al. unpublished'). Eger ral, insecticide, parasite, predator) c o u l d be a p • (1981) reported a model that predicts t h e overwin• plied. T h e output of M O T H Z V - 2 w a s in t h e form of ter mortality of diapausing p u p a e d u e to low tables or graphs of the daily n u m b e r s of Heliothis temperature. T h e s e models will eventually permit spp of e a c h stage. the prediction of n u m b e r s of surviving overwinter• T h e three crop models w e r e t e m p e r a t u r e - ing p u p a e a n d the timing of e m e r g e n c e . dependent a n d used a degree-day c o n c e p t to pre• dict crop phenology events s u c h as first square, Heliothis Population Model: MOTHZV boll, a n d ope n boll. T h e s e w e r e then u s e d to predict the relative attractance of the c r o p to females, a Hartstack et al. (1973) reported the c o n c e p t of a factor affecting oviposition. No yield prediction w a s simple model of the Heliothis spp (Fig. 1). Hartstack possible. E a c h crop required a separate run of the a n d Hollingsworth (1974) c o n v e r t e d this m o d e l model; however, Heliothis zea adults predicted to c o n c e p t to m a t h e m a t i c a l equations, a n d with the migrate out of c o r n or s o r g h u m were held in a use of a c o m p u t e r w e r e able to m a k e predictions of vector that c o u l d be used as input for a subsequent the n u m b e r a n d timing of future adults. D e v e l o p • run of cotton. In this situation, the population of ment times, using a d e g r e e - d a y c o n c e p t , w e r e c a l • adults migrating into cotton w a s adjusted by the culated as total generation lengths (adult to adult) ratio of hectares of cotton to hectares of c o r n a n d rather than being divided into various life stages. sorghum in the region. (For detailed description see Rates of increase w e r e input as constants for e a c h Hartstack et al. 1973, 1976a.) day, based on light-trap data collected at College Station over a 3-year period. Moonlight w a s the only other factor that affected rate of increase. MOTHZV-3 Predictions of timing a n d size of future generations w e r e very a c c u r a t e for College Station, but this In 1978, M O T H Z V - 2 w a s revised. As reported from regression-type model l a c k e d the versatility extensive studies by Q u a i n t a n c e a n d Brues (1905), n e e d e d for use at other locations. T o w n s e n d (1973), a n d by Baldwin et al. (1974), the larval stage of Heliothis spp c a u s e s the most d a m • age to fruiting cotton. Therefore a Heliothis d a m a g e MOTHZV-2 model was a d d e d to M O T H Z V - 2 , a n d the original cotton model w a s replaced by a m o r e d y n a m i c Hartstack et al. (1976a) presented a detailed d e s • crop model, SIMPLECOT, for cotton fruiting b e h a v • cription of M O T H Z V - 2 , a d e s c e n d a n t of the original ior, based on a model d e v e l o p e d by Wilson et al. M O T H Z V , w h i c h incorporated considerably m o r e (1972). This revision, M O T H Z V - 3 , allows t h e user detailed population and physiology algorithms (Fig. to study c h a n g e s in cotton yield c a u s e d by Helio• 2) a n d included three simple c r o p m o d e l s — c o r n , this, a n d makes new a n d m o r e c o m p l e x studies cotton, a n d s o r g h u m . T h e F O R T R A N c o m p u t e r also possible. p r o g r a m for M O T H Z V - 2 consisted of a main c o m • T h e cotton model c a n be adjusted for a particular puter p r o g r a m a n d 16 subroutines. simulation by varying the t w o input parameters, a Predictions of timing a n d size of future g e n e r a • variety factor, a n d yield. A base run with no d a m a g e tions of Heliothis spp w e r e m a d e by using e x p e c t e d c a n be made. T h e effect on yield of various insect (long-term average) temperatures a n d e x p e c t e d or populations or p e s t - m a n a g e m e n t decisions c a n be predicted c r o p phenology. Simulations w e r e initial• studied by c o m p a r i n g subsequent runs with t h e ized with input of either eggs or moths, a n d t h e base run or to e a c h other. population w a s carried through as m a n y g e n e r a • tions as occur during o n e season. A b o o k k e e p i n g s y s t e m r e c o r d e d the n u m b e r of eggs, first- to third- A Statewide Extension Program: instar larvae, fourth- a n d fifth-instar larvae, pupae, BUGNET

1J.D. Lopez, A W . Hartstack, and J A Witz. 1982, Diapause development of the tobacco budworm in Central Texas. B U G N E T is a computerized p e s t - m a n a g e m e n t

5 3 I n p u t Catch per trap Start corn, cotton, e t c . D a y " A "

Convert trap catch to moths per acre

Calculate generation Store Day "B" length expected from Next generation D a y " A " day n o .

Calculate rate of increase expected from (Rate of increase in each crop) x (No. moths/ Day "A" to Day "B" for acre in crop) e a c h crop

Sum projected (Projected population) x populations in % of crop in area e a c h crop

Calculate moonlight effect and adjust projected population

Calculate longevity of projected population and store accordingly

Y e s O u t p u t L a s t day population projected and Day "B"

N o

Go to next day Stop

Figure 1. Flowchart of the first version of the MOTHZV model for prediction of Heliothis spp populations.

5 4 Figure 2. Flowchart showing the complexity of the MOTHZV-2 model.

5 5 delivery system in Texas, developed by entomolo• The first data were mailed to College Station by gists of the Texas Agricultural Extension Service the county extension entomologist about 30 days and research cooperators, to make computer mod• after the traps were installed; thereafter, data we r e els available to the personnel of the Extension Ser• forwarded whenever it seemed necessary to vice and thereby to the public. The MOTHZV model update a forecast, usually every 7 to 14 days. As and the other BUGNET programs are currently soon as the data arrived at College Station, they being used by producers across the state for pest- were punched on computer cards, and MOTHZV-2 control decision-making. (stored on-line at the Texas A & M Data Processing A statewide pest-management plan for Texas Center) was run to forecast the timing and size of (Frisbie and Adkisson 1975) was proposed in 1974; the expected egg and larval populations of H.zea the pilot action programs in 1973,1974, and 1975 a n d H.virescens through the season. This output proved so encouraging in maintaining the profita• was then marked to the extension entomologist bility of cotton and sorghum production that the and other interested personnel, with the caution Texas Association of Cotton Producers asked the that predictions were to be used only as trend State's extension service, experiment station, and indicators and not as predictions of actual numbers the Texas Department of Agriculture to implement in specific fields. the plan statewide. In 1976, three light traps (Hollingsworth and This statewide plan, which began in 1976, con• Hartstack 1972) were installed at each of five test sisted of 10 subplans developed by individual sub• locations. The forecasts in 1976 were within 3 days committees. Nine of the plans were geographically of the actual peaks in the field. Figure 3 shows a based on the nine cotton and sorghum-producing comparison of the June forecast of H. zea oviposi- areas of Texas. The tenth, TAMU-BUGNET, was tion with the actual field egg counts in the Hillsboro, involved with the potential of a computer-based system of forecasting insect-pest populations and crop yields. The goal of BUGNET is to aid farmers in making decisions concerning insect control and M O T H Z V - 2 crop management. prediction (2 June)

Actual egg counts BUGNET Phase One (Hillsboro Area)

The BUGNET program was initiated to make var• ious computer applications, including MOTHZV, available to the county extension entomology spe• cialists. To acquire the necessary input informa• tion, insect light traps were installed at each location early enough to enable monitoring of moth emergence from the diapausing (overwintered) pupae. This timing varied from February in the Rio Grande Valley to May in the Rolling Plains area. Traps were located within early-season hosts of H. zea—corn or s o r g h u m or b o t h — d e p e n d i n g on which was the major crop in the area. When cotton began to square or when the corn or sorghum matured, the traps were moved into cotton. Additional input data gathered by the specialist for the BUGNET version of MOTHZV-2 were: (1) 20 10 30 19 minimum and maximum daily temperature; (2) J u n e J u l y A u g u s t planting date, emergence date, and date of first fruit (silk, bloom, square, boll) for each of three crops Figure 3. An example of the MO THZV-2 predic- (corn, sorghum, cotton) in the area; (3) the percen - tion (2 June) compared with actual field counts tage of each of the three crops in the area (one of Heliothis spp eggs in the Hillsboro area, county or more). Texas, USA, 1976.

5 6 Texas, area. T h e s u c c e s s f u l results of this pro• Although an insecticide application w a s never gram's first year w e r e reported by Hartstack et al. based solely on M O T H Z V , the a d v a n c e k n o w l e d g e (1977). of possible insect infestations alerted p r o d u c e r s to I n 1977 t h e B U G N E T - M O T H Z V p r o g r a m w a s intensify scouting efforts. In irrigated areas, s u c h e x p a n d e d from 5 to 15 areas. T w o or three electric a d v a n c e knowledge w a s valuable in timing irriga• grid traps (Wolf et al. 1972) baited with Virelure tion (Slosser 1979). Since the rapid plant growth (Tumlinson et al. 1975; Hendricks et al. 1977), a and lush foliage that immediately follow irrigation synthetic attractant for H. virescens, w e r e installed are extremely c o n d u c i v e to Heliothis e g g laying, at e a c h location in addition to the light traps. T h e avoiding irrigation at times w h e n insect populations p h e r o m o n e - t r a p c a t c h e s w e r e u s e d as inputs to are high c a n be an effective control measure. M O T H Z V - 2 for predictions of H. virescens In areas w h e r e other pests are problems prior to oviposition. Heliothis, it is important to stop pesticide treatment In 1978, M O T H Z V - 2 w a s replaced by M O T H Z V - for early-season pests several w e e k s before Helio• 3; in 1979, the grid traps w e r e replaced by c o n e this populations build up. A d v a n c e knowledge of traps (Hartstack et al. 1979) that required no elec• probable buildups helps determine the best insecti• tricity a n d w e r e m u c h m o r e versatile. T h e program cide cutoff date, to enable beneficial insects to has continued to operate at about 15 locations recover from the treatment a n d r e a c h a level effec• s i n c e 1977. tive for control of Heliothis. A statement issued by the T e x a s Agricultural BUGNET Phase Two Extension Service in 1979 pointed out that M O T H Z V h a d enjoyed w i d e s p r e a d u s e over 3 A s e c o n d p h a s e of the overall B U G N E T program, years; in 1979 alone, 5740 cotton producers in 91 begun in 1977, attempted to put c o m p u t e r power counties had used this tool to help m a n a g e 4 0 6 9 directly into the hands of the county extension spe• 300 acres (1 646 789 ha) of cotton, for a c o m b i n e d cialist. IBM 5100 minicomputers were installed at net profit of $4 967 000. In addition, it brought three locations to test the feasibility of their use by intangible benefits, s u c h as p e a c e of mind, w h i c h field personnel. M O T H Z V - 4 , a simplified version of could not be m e a s u r e d in dollars. M O T H Z V - 3 , written in APL, w a s sent to the field in 1979, to be used on the minicomputers; although this version lacked m u c h of t h e versatility of T h e F u t u r e for M O T H Z V M O T H Z V - 3 , it c o u l d successfully predict timing of Heliothis spp oviposition. Although the value of this work entailing a systems In 1980, B U G N E T a d d e d 11 m o r e m i n i c o m p u • a p p r o a c h remains to be fully tested a n d evaluated ters a n d u p g r a d e d the original three. Other soft• for p e s t - m a n a g e m e n t applications in cotton, w a r e p a c k a g e s have also bee n m a d e available to benefits have already been realized in identifying users: a Peanut Leaf Feeder Model, P e c a n Produc• research gaps and priorities. M a n y i m p r o v e m e n t s tion G a m e , Adult P e c a n Weevil Mortality, P e c a n need to be m a d e in the model itself. While t h e Weevil Static Threshold M o d e l , S o r g h u m M i d g e predicted timing was close, the n u m b e r s predicted Static T h r e s h o l d Model, Insecticide Compatibility were not very accurate. Chart, Cotton Production G a m e s , IBM Statistics Increasing emphasis is now being p l a c e d on t h e Pack, a n d a Boll Weevil M o d e l. use of beneficial insects. Natural predators a n d parasites are being studied to determine their o c c u r r e n c e a n d ability to control pest species; MOTHZV on BUGNET: Results however, basic biological data available on benefi• T h e first year, forecasts w e r e of limited use to cial species are limited. M e t h o d s to m a n a g e a n d farmers, both b e c a u s e there w a s doubt about their increase natural beneficials are being considered. reliability a n d b e c a u s e populations w e r e low and of Researchers are also looking at m e t h o d s of rearing little e c o n o m i c importance e x c e p t for a few local• a n d distributing beneficial species as an alternative ized outbreaks. But c o n f i d e n c e in the model has pest-control t e c h n i q u e (Ridgway et al. 1980). g r o w n steadily e a c h year since, a n d over t h e 3 I m p r o v e d m e t h o d s of sampling beneficial popula• years 1 9 7 7 - 7 9 , the predicted e g g peaks w e r e tions to determine their o c c u r r e n c e a n d n u m b e r within 4 d a y s of the actual field e g g c o u n t s about are required before this m e t h o d of pest control c a n 7 0 % of the time. b e c o m e practicable on a large scale.

57 MOTHZV-3 does not consider the effect of rain• Bulletin 1144, Texas A&M University, College Station, fall and soil moisture on the growth of the crop or T e x , U S A . insect. Because lush crop growth has a marked effect on Heliothis oviposition, it affects the timing BROWN, L.G., McCLENDON, R.W., and JONES, J.W. and size of egg peaks. Mortality of eggs and larvae 1 9 7 9 . Computer simulation of the interaction between is also affected by moisture conditions, a factor not the cotton crop and insect pests. Transactions of t h e considered in the model. However, before these American Society of Agricultural Engineers 22(4): 771 - 7 7 4 . factors can be incorporated and used successfully, better methods of monitoring rainfall and soil mois • BUTLER, G.D. 1976. Bollworm: development in relation ture are needed. Perhaps remote sensing will be to temperature and larval food. Environmental Entomol • the answer. ogy 5: 520-522. One of the most important inputs to the present model is early-season trap catches. Light traps BUTLER, G.D., and HAMILTON, A.G. 1976. D e v e l o p • (Hartstack et al. 1971, 1973) have been one of the ment time of Heliothis virescens in relation to constant best ways to monitor Heliothis adults; however, temperature. Environmental Entomology 5: 759-760. each trap requires an electrical power source, BUTLER, G.D., HAMILTON, A.G., and PROSHOLD, which often interferes with field operations. Light- F.I. 1 9 7 9 . Development times of Heliothis virescens a n d trap catches are also difficult to identify at times. H. subtlexa in relation to constant temperature. Annals of Experience with MOTHZV-BUGNET has shown the Entomological Society of America 72: 263-266. that at least three, and perhaps five to ten, traps are

required to properly monitor Heliothis adults in an EGER, J.E., Jr. 1981. Factors affecting winter survival of area. Because operating so many light traps would Heliothis virescens (Fabricius) a n d Heliothis zea ( B o d d i e ) be very expensive, time-consuming, and trouble- (Lepidiptera: Noctuidae), and subsequent developmen t some, numbers have usually been sacrificed for on wild spring hosts. Ph.D. dissertation, Texas A&M U n i • convenience. Even locating the traps in the proper versity, College Station, Tex, USA. crop and place has been difficult because of power requirements, and this inadequacy, plus irregular DeMICHELE, D.W., and BOTTRELL, D.G. 1976. S y s • tems approach to cotton insect pest management. Pag e s servicing, has contributed substantially to predic• 1 0 7 - 1 3 2 in Integrated pest management. New York, USA: tion errors. Plenum Press. New pheromone traps (Hartstack et al. 1979) and synthetic sex pheromones (Klun et al. 1979) for FRISBIE, R.E., and ADKISSON, P.L. 1975. S u m m a r y : both H. zea a n d H. virescens have recently been Statewide pest management plan. Texas Agricultural developed; these should provide the pest manager Extension Service, Texas A&M University System, Col • or producer with a convenient and effective tool for lege Station, Texas, USA. monitoring Heliothis adults. The traps are highly efficient, simple to construct, inexpensive, and por• HARTSTACK, A.W., Jr., and HOLLINGSWORTH, J.P. 1974. A c o m p u t e r m o d e l for p r e d i c t i n g Heliothis p o p u l a • table (requiring no power). Only the single species tions. Transactions of the American Society of Agri c u l t u • for which the trap is baited is attracted and caught, ral Engineers 17(1): 112-115. making identification and counting quick and easy. The pheromones are now commercially available; HARTSTACK, A.W., Jr.,and WITZ. J.A. 1982. E s t i m a t • therefore, the proper array of five to ten traps ca n ing field populations of tobacco budworm moths from be located within the proper crops and should not pheromone trap catches. Environmental Entomology (In be difficult to monitor. As an added bonus, phero• press). mone traps also detect spring emergence of moths 2 or 3 weeks earlier than light traps, which should HARTSTACK, A.W., Jr., HOLLINGSWORTH, J.P., give more precision to forecasts. RIDGWAY, R.L., and HUNT, H.H. 1971. Determination of trap spacings required to control an insect popul a t i o n . Journal of Economic Entomology 64(5): 1090-1100.

References HARTSTACK, A.W., Jr., HOLLINGSWORTH, J.P., RIDGWAY, R.L., and COPPEDGE, J.R. 1973. A p o p u • BALDWIN, J.L., WALKER, J.K., GANNAWAY, J.R., lation dynamics study of the bollworm and the tobac c o and NILES, G.A. 1974. Boltworm attack on experimental budworm with light traps. Environmental Entomology 2(2): semidwarf cottons. Texas Agricultural Experiment Sta t i o n 2 4 4 - 2 5 2 .

58 HARTSTACK, A.W., Jr., WITZ, J.A., and RIDGWAY, KLUN, J.A., PLIMMER, J.R., BIERL-LEONHARDT, R.L. 1 9 7 5 . Suggested applications of a dynamic Helio• B.A., SPARKS, A.N., and CHAPMAN, O.L. this model (MOTHZV-1) in pest management decision 1979. Trace chemicals: The essences of sexual com• making. Pages 118-122 in Proceedings, Beltwide Cotton m u n i c a t i o n s y s t e m in Heliothis spp. Science 204:1328. Producers Research Conference. KNIPLING, E.F. 1979. The basic principles of insect HARTSTACK, A.W., Jr., WITZ, J.A., HOLLINGS- population suppression and management. U.S. Depart• WORTH, J.P., RIDGWAY, R.L, and LOPEZ, J.D. ment of Agriculture Handbook 512, Washington DC, USA . 1976a. MOTHZV-2: A computer simulation of Heliothis 6 5 9 pp. zea a n d Heliothis virescens population dynamics. U.S. Department of Agriculture Users' Manual ARS-S-127, LOGAN, J.A., STINNER, R.E., and RABB, R.L. 1979. A Washington DC, USA. 55 pp. descriptive model for predicting spring emergence of Heliothis zea populations in North Carolina. Environmen• HARTSTACK, A.W., Jr., WITZ, J.A., HOLLINGS- tal Entomology 8: 141 -146. WORTH, J.P., and BULL, D.L. 1976b. SPERM. A sex pheromone emission and response model. Transactions McKINION, J.M., BAKER, D.N., HESKETH, J.D., and of the American Society of Agricultural Engineers 19(6): JONES, J.W. 1975. SIMCOT II. A simulation of cotton 1 1 7 0 - 1 1 8 0 . growth and yield. Pages 27-82 in Computer simulation of a cotton production system. U.S. Department of Agri c u l • HARTSTACK, A.W., Jr., HENSON, J.L., WITZ, J.A., ture User's Manual ARS-S-52, Washington DC, USA. JACKMAN, J.A., HOLLINGSWORTH, J.P., and FRIS- BIE, R.E. 1977. The Texas program for forecasting Heli• POTTER, M.F., HUBER, R.T., and WATSON, T.F. othis spp. infestations on cotton. Pages 151-154 in 1 9 8 1 . Heat unit requirements for emergence of overwin• Beltwide Cotton Producers' Research Conference. tering tobacco budworm, Heliothis virescens, in Arizona. Environmental Entomology 10: 543-545. HARTSTACK, A.W., Jr., WITZ, J.A., and BUCK, D.R. 1979. Moth traps for tobacco budworm. Journal of Eco• QUAINTANCE, A.L., and BRUES, C.T. 1905. T h e c o t • nomic Entomology 72(4): 519-522. ton bollworm. U.S. Department of Agriculture Bureau of Entomology Bulletin 50, Washington DC, USA. HARTSTACK, A.W., Jr., WITZ, J.A., and LOPEZ, J.D. 1982a. Predicting the timing of the spring emergence of RIDGWAY, R.L., ABLES, J.R., GOODPASTURE, C, overwintered populations of Heliothis spp. (In press). and HARTSTACK, A.W. 1981. Trichogramma a n d its utilization for crop protection in the United States. In Pro• HARTSTACK, A.W., Jr., LOPEZ, J.D., STERLING, ceedings, Soviet-American Conference on Use of Bene • W.L., KING, E.G., MULLER, R.A., and WITZ, J.A. ficial Organisms in Control of Crop Pests. St. Paul, M i n n . , 1982b. Long range spring migration of Heliothis zea i n d i • USA: American Phytopathological Society. cated. (In press). SLOSSER, J. 1980. Irrigation timing for bollworm man• HENDRICKS, D.E., HARTSTACK, A.W., and agement in cotton. Journal of Economic Entomology SHAVER, T.N. 1977. Effect of formulations and dis• 73(2): 346-349. pensers on attractiveness of virelure to the tobacco b u d - worm. Journal of Chemical Ecology 3: 497-506. STINNER, R.E., GUTIERREZ, A.P., and BUTLER, G . D . 1974. An algorithm for temperature-dependent HOLLINGSWORTH, J.P., and HARTSTACK, A.W. growth rate simulations. Canadian Entomologist 106: 1 9 7 2 . Effect of components on insect light trap perfor• 5 1 9 - 5 2 4 . mance. Transactions of the American Society of Agricu l • tural Engineers 15(5): 924-927. STINNER, R.E., RABB, R.L., and BRADLEY, J.R. 1974. Population dynamics of Heliothis zea and H. vires- JONES, J.W., BOWEN, H.D., STINNER, R.E., BRAD- cens in North Carolina: a simulation model. Environmen- LEY, J.R., and BACHELER, J.S. 1977. Simulation of tal E n t o m o l o g y 3 : 1 6 3 - 1 6 8 . boll w e e v i l p o p u l a t i o n s a s i n f l u e n c e d b y w e a t h e r , c r o p status, and management practices. Transactions of th e TOWNSEND, J.R. 1973. Economic Threshold studies American Society of Agricultural Engineers 20(1): 121- of Heliothis spp. on cotton. M.S. Thesis, Department of 125. Entomology, Mississippi State University, Miss, USA. 7 2 pp. JONES, J.W., BROWN, L.G., and HESKETH, J.D. 1 9 8 0 . COTCROP: A computer model for cotton growth and yield. Chapter 10 in Predicting photosynthesis for TUMLINSON, J.H., HENDRICKS, D.E., MITCHELL, ecosystems models. West Palm Beach, Fla, USA: CRC E.R., DOOLITTLE, R.E., and BRENNAN, M.M. Press. 1975. Isolation, identification and synthesis of the sex

5 9 pheromone of the tobacco budworm. Journal of Chemica l Ecology 1:203-214.

WATSON, F.L. 1973. T h e o p t i m a l c o n t r o l of Lygus hes- perus on cotton. Unpubl. Ph.D. thesis, University of Ariz• ona, Ariz, USA. 207 pp.

WILSON, A.Q., HUGHES, R.D., and GILBERT, N. 1 9 7 2 . The response of cotton to pest attack. Bulletin of Entomological Research 61: 405-414.

WILSON, A.G.L., LEWIS, T., and CUNNINGHAM, R.B. 1979. Overwintering and spring emergence of Heli- othis armigera (Hubner) (Lepidoptera: Noctuidae) in the Namoi Valley, New South Wales. Bulletin of Entomolog i • cal Research 69: 97-109.

WITZ, J.A. 1973. Integration of systems methodology and scientific research. Agricultural Science Review 1 1 : 3 7 - 4 8 .

WOLF, W.W., TOBA, H.H., KISHABA, A.N., and GREEN, N. 1972. Antioxidant to prolong the effective• ness of cabbage looper sex pheromone in the field. J o u r • nal of Economic Entomology 65:1039-1041.

6 0 Migration as a Factor in Heliothis Management

J.R. Raulston, W.W. Wolf, P.D. Lingren, and A.N. Sparks*

Abstract

Many studies have demonstrated the mobility ot our Heliothis pest species through their capability to extend their ranges hundreds ot kilometers beyond their over-wintering ranges. Other studies have also yielded circumstantial evidence of their long-range movement within the confines ot their indigenous ranges, even though definitive studies have not yet been made of such movement between habitats. The array of techniques developed for studying movement of locusts and spruce budworms provide models upon which to base more intensive studies of Heliothis spp movement. A better understanding of both long- and short-range movement of the insects is required to functionally define areas of treatment for testing suppression theories that extend beyond the boundaries of our cropping system and utilize an integrated and holistic approach to population suppression.

Since the advent of efficient insecticides and upon scheduled insecticide treatments to protect methods of application, concepts for controlling his crop. pest insect populations have been concentrated With better understanding of the negative mostly upon field-to-field management following aspects of pesticide use, in relation to both the appearance of the insect or its damage to the crop. environment and the control of the target species Jackson (1979) points out that much of the itself, has arisen a need and demand for pest- insecticide-usage technology is implemented by management systems that optimize naturally the individual grower, who historically has utilized occurring suppression mechanisms and utilize insecticides with little understanding of the nega• nonpesticide control treatments. Metcalf (1980), tive effects that are triggered by such application. reviewing the pesticide treadmill syndrome, dis• As a consequence, many insect-control programs cusses the philosophical changes that are re• were developed that placed the grower on an sulting in the development of integrated insecticide treadmill, making him totally reliant pest-management systems on a worldwide basis. For effective timing of control measures, such sys• tems require accurate prediction of population *U.S. Department ot Agriculture, Agricultural Research Service, buildups or outbreaks, and a thorough knowledge Cotton Insects Research, Brownsville, Texas; Grain Insects of the pest species population dynamics. We there• Research, Tifton, Georgia; Western Cotton Research Laboratory, fore need to determine the movement capabilities Phoenix, Arizona; and Grain Insects Research, Tifton, Georgia; of populations both on a regional and on a local respectively.

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. 61 scale. Further, we need a better understanding of source in either northwestern Spain or north Africa, the parameters that influence movement, including a distance of 800 to 1600 km. the chronology of croppings systems, which deter• Documentation of emigration or immigration mines host availability as discussed by Lopez within the confines of the overwintering range of t h e (1976), and the development of meteorological species is confounded by the presence of indigen• events that offer modes of transport such as those ous populations from which immigrants are difficult described by Beckman (1973). or impossible to distinguish. Indeed, this led Phillips (1979) to declare that in the state of Arkansas, USA, for a 6-year period from 1972 to 1978, if immigra• tion of H. zea had occurred, it had done so with no Evidence of Heliothis Spp net effect on the seasonal population dynamics of Movement the species. However, several studies have indi• c a t e d Heliothis spp dispersal or their ability to dis• The physical displacement of Heliothis over rela• perse within their indigenous range. tively long distances has been referred to by sev• Callahan et al. (1972) placed 15 light traps at eral investigators. Although these studies have not varying heights on a 318-m television tower at Pel- f o l l o w e d Heliothis spp movement from a degener• ham, Georgia, to study the vertical distribution of H. ating habitat over a migratory path to a more attrac• zea. These traps were constructed so that only tive habitat, they have yielded circumstantial insects flying above them could detect the light an d evidence of the capability of Heliothis for long- thus be attracted to the traps. These investigators range movement. c a p t u r e d H. zea males and females in each of the Snow and Copeland (1971) surveyed the Coop• traps, including the one at 318 m, and observed a erative Economic Insect Reports in the USA for a relatively even distribution in all traps above 83 m. 19-year period, from 1951 to 1969, and observed During peak flight periods, over 50% of all insects that both in the eastern and western parts of the captured were H. zea, and they concluded that the country, Heliothis zea (Boddie) had been reported moths were probably migrating. as overwintering roughly up to 45°N. Through the Sparks et al. (1975) placed light traps on mid-continent area, where more extreme fluctua• unmanned oil rigs in the Gulf of Mexico south of tions in temperature are normally experienced, the Jeanerette, Louisiana, and captured H. zea at all northern limit of winter survival appeared to corre s • trap locations, with a decreasing concentration pond roughly to 40°N. These authors concluded gradient occurring from those traps closest to that the range of H. zea winter survival corres• shore (43 km) to those most distant (160 km). Eva• ponded roughly to those regions receiving the last luation of weather data collected on the oil rigs led spring freeze prior to April 30. However, Hardwick Sparks and associates to conclude that these (1965) in his monograph on the corn earworm moths were being transported on southbound cool complex, states that H. zea in some years is pres• fronts. ent as far north as 52°N, indicating that in North Snow et al. (1969) labeled a naturally occurring A m e r i c a , H. zea extends its range 600 to 1200 km population of H. zea on corn with P32 and observed over about a two-generation period. the dispersal pattern over the 134 km2 island of St. Hardwick (1965) further states that the indigen• Croix, U.S. Virgin Islands. Labeled H. zea dispersed ous range of Heliothis armigera (Hb.) probably cor• over the entire island and concentrated around responds roughly to 40o north and south latitude, areas with attractive host plants. In a later study thus approximating the overwintering range of H. involving the release of sterile Heliothis virescens zea observed in the USA. Like H. zea, H. armigera (F.) a n d H. zea on St. Croix, Haile et al. (1975) apparently is able to extend its range well beyond operated pheromone traps for both species on the that at which it is capable of overwintering during its islands of Vieques and St. Thomas. Released reproductive phase. Hardwick (1965) lists the most insects of both species dispersed to these islands, northerly record for the species as being Narva, which are located at a distance of 67 km (Vieques) Estonia, in the USSR at about 59°N. French and and 61 km (St. Thomas) down- or cross-wind from Hurst (1969) documented the arrival of H. armigera St. Croix, and the investigators concluded that in the British Isles at about 51°N in July 1968, an d movement of indigenous populations between through correlation with meteorological events, islands was highly probable. were able to backtrack the insects to their probabl e Other studies have documented the dispersal of

6 2 Heliothis spp over relatively long distances within N = 3 6 0 t h e continental USA. o Sparks (1972) released marked laboratory-reared H. zea adults near Tifton, Georgia, a n d c a p t u r e d moths at a 2 5 - k m distance 15 f r o m the release site after o n e night, a n d at a dis• t a n c e of 72 km over a period of 1 to 4 days. H e n • dricks et al. (1973) studied the dispersal of 10 laboratory-reared H. virescens adults with phero- m o n e traps near Brownsville, Texas, a n d d e m o n • strated their m o v e m e n t up to 112 km d o w n w i n d of the prevailing w i n d pattern. Also, males w e r e c a p • 5 tured at a distance of 25 km against prevailing win d patterns; however, s i n c e no attempt w a s m a d e to correlate trap captures on a temporal a n d spatial basis with meteorological events, o n e c a n n o t rule 5 10 1 5 20 Trap N o . out the possibility of these moths having dispersed on storm fronts or other meteorological p h e n o • Figure 1. Recapture of fluorescent dye-marked m e n a that c o u l d result in temporary w i n d shifts Heliothis virescens in Lower Rio Grande Phero- from prevailing patterns. mone trap line. Males were released near San In 1979, Raulston studied the m o v e m e n t of Fernando, Tamaulipas, Mexico, in May 1979. native H. virescens male moths, using a capture, mark, a n d recapture method. T h e s e males were collected from a line of 26 wind-oriented p h e r o - T h e a v e r a g e temperature at 3 0 0 0 m tor the m o n t h m o n e traps (Raulston et al. 1980) situated in the w a s 9.4°C, w h i c h is well above the flight threshold Lower Rio G r a n d e Valley of Texas, extending east t e m p e r a t u r e of Heliothis spp observed by C a r p e n • to west a distance of 80 km. T h e moths were s u b • ter et al. (1982). 1 sequently m a r k e d by dusting t h e m with Day-glo® To alleviate the problem of mark contamination, fluorescent powder, and released near San Fer- three releases were m a d e in J u n e a n d July utilizing nando, T a m a u l i p a s , M e x i c o , a d i s t a n c e of 160 km black or blue felt tip markers to spot-mark individual south of the Valley. Altogether, 16 0 0 0 moths w e r e wings on the released insects. From a total of 18 released on two o c c a s i o n s in May, a n d recapture 0 0 0 males released at San Fernando, only four was o b s e r v e d in the trap line situated in the Valley. w e r e recaptured in the Valley trap line. Following Since subsequent observations indicated that the first release on 7 J u n e until the s e c o n d release recaptured m a r k e d moths c o n t a m i n a t e d u n • on 14 June, no windflow at a direction greater than m a r k e d ones, no reliable estimate c a n be m a d e of 170° w a s observed below an altitude at w h i c h the the total number of moths recaptured from the temperature w a s a b o v e 4.4°C. However, o n e release point. However, w h e n the p e r c e n t a g e of m a r k e d male w a s recaptured, e v e n t h o u g h n o total m a r k e d moths o b s e r v e d w a s calculate d for favorable winds had o c c u r r e d to transport released e a c h trap (Fig. 1), t w o major areas of recapture moths into the main area of the trap line. Following were indicated at traps 9, 10, a n d 18. T h e s e three the s e c o n d release on 14 J une , favorable w i n d s traps a c c o u n t e d for 4 0 % of the o b s e r v e d m a r k e d w e r e noted on 17 J u n e b e t w e e n an altitude of 9 0 0 moths. A s s u m i n g the moths m o v e d primarily d o w n - a n d 2 7 0 0 m, a n d t w o moths w e r e recaptured, o n e wind, a w i nd direction b e t w e e n 180° a n d 210° on 18 J u n e a n d o n e on 20 June. Following the third w o u l d be required to transport moths from the release on 22 J une, favorable winds w e r e noted on release site to t h e trap-line area. Data s h o w n in two o c c a s i o n s (22 a n d 25 July), a n d o n e m o t h w a s T a b l e 1, taken from p s e u d o - a d i a b a t i c charts at recaptured on 31 July. T h e w i n d shifts that Brownsville, Texas, indicate that favorable w i n d - o c c u r r e d after M a y w o u l d appear to r e d u c e t h e flows for s u c h transport o c c u r r e d on M a y 10, 1 1 , possibility of transport from the release site into the 12, 18 to 2 2 , a n d 26 to 31 at altitudes below 3 0 0 0 m. Valley. Only 1 6 % of the days in J u n e h a d favorable winds, while 5 1 , 50, a n d 5 4 % of t h e days in M a r c h , April, a n d M a y respectively, h a d favorable winds.

1. Mention of a commercial product does not constitute an endor- B e t w e e n 1 August a n d 6 September 1979, 13 sement of that product by the USDA. releases of a total of 44 0 0 0 males w e r e m a d e

6 3 Table 1. Occurrence of winds2 favorable for the transport of Heliothis virescens males from a release point south of San Fernando to the Lower Rio Grande Valley trap line, May 1979.

A l t i t u d e M a y ( m ) 1 0 1 1 1 2 1 3 1 4 1 5 1 6 1 7 1 8 1 9 2 0 2 1 2 2 2 3 2 4 2 5 2 6 2 7 2 8 2 9 3 0 3 1

0 3 0 0 + 6 1 0 + + + + + 9 1 0 + + + + + + + + + + 1 2 3 0 + + + + + + + + + + 1 5 2 0 + ------1 8 3 0 + + + + + + + + 2 1 3 0 + + + + + + + 2 4 4 0 + + + + + + + + + 2 7 4 0 + + + + + + + + 3 0 4 0 - + + - - - - + a. + = wind direction between 180° and 210°; - = mi ssing data.

about 30 km north of Brownsville, to study possible cultural Station, National Institute of Agricultural movement from the Valley area to the north. A line Investigations, by Ing. Felipe Silguero from 1974 to of five wind-oriented traps was extended from 1980. The Brownsville area normally has about 120 Chapman Ranch to Alice, Texas, for this study. 000 ha of cotton, which is planted in late February (These traps were operated by Dr. John Benedict, and early March and begins fruiting in early May. Texas Agricultural Experiment Station, Corpus The San Fernando area is primarily rangeland and Christi, Texas). A distance of 130 km separated the dryland sorghum, while Tampico grows crops such release point from the trap line, and a wind direction as maize, tomatoes, soybean, chillies, safflower, between 150° and 170° was required to transport and sugarcane, none of which support major popu• moths to the trap-line area. Five males were recap• lations of H. virescens. However, the region tured in the Chapman Ranch-Alice trap line; none between San Fernando and Tampico and areas in the Valley trap line south of the release point. south of Tampico support large populations of two Radiosonde data from Brownsville (Table 2) indi• wild hosts. Abutilon trisulcatum (Jacq.) and Bastar- cate 49% of the readings below 3000 m were within dia viscosa (L), in the spring and fall. the range of favorable transport. The recapture of The major spring trap-capture peak at San Fer- so few males may have resulted from a lack of nando occurred during the months of March attractive host plants in the trap-line area; however, through May, which also corresponds with major the availability of an aerial transport mechanism trap capture in the Brownsville area, well before was demonstrated. cotton is available to produce Heliothis Studies of the population dynamics of H. vire- populations. scens and meteorological patterns occurring Figure 3 shows surface synoptic weather maps within the region have yielded further circumstan• of the U.S. and pseudoadiabatic charts from tial evidence suggesting the possibility of moth Brownsville, Texas, for March 17 and 23 of 1980, transport from northeastern Mexico to southern which typify the weather patterns for the region Texas and beyond. during this period of the year. The March 17 synop• Pheromone- and light-trap data are shown in tic map shows moderate low-level winds (5 to 7.5 Figure 2 for Brownsville, Texas, and San Fernando m/sec) with the potential for surface air transport and Tampico, Tamaulipas, Mexico. Data from from southerly components, southwest to south- Brownsville and San Fernando were obtained from east, northward across coastal Texas and north- pheromone traps from 1978 through 1980, while westward into the Mississippi River Valley, ahead of data from Tampico were obtained from light traps an approaching cold front. The pseudo-adiabatic operated at the Las Huastecas Experimental Agri• chart for that date at Brownsville further illustrates

6 4 T a b l e 2 . O c c u r r e n c e o f w i n d s * f a v o r a b l e f o r t h e t r a n s p o r t of Heliothis virescenes mala* from a release point near Arroyo City to a trap line between Chapman Ranch and A l i c e , T e x a s , 1 A u g t o 9 S e p t 1 9 7 9 .

A l t i t u d e ( m )

D a t e 0 3 0 0 6 1 0 9 1 0 1 2 3 0 1 5 2 0 1 8 3 0 2 1 3 0 2 4 4 0 2 7 4 0 3 0 4 0

A u g 1 + + + + + + + - 2 + + + + + - + + + + - 3 + + + + + - + + + + - 4 + + + - + + + + - 5 + - 6 + - - 7 + + + + - + + - 8 + + - - 9 + + + + 1 0 + + + + + + + - 1 1 + + + + + - + + + + + 1 2 + + + + + - + + + + - 1 3 + + + + + + + + - 1 4 + + + + - + + + + - 1 5 + + 1 6 + + + + + + + + 1 7 + + 4 + + - 1 8 + + + + - - 1 9 + + + + + + + + - 2 0 + + + + + + + + - 2 1 + + + + + + + + - 2 2 + + + + + - + + + + - 2 3 + + + + + - 2 4 + - 2 5 - 2 6 + + + + + - 2 7 + 2 8 - 2 9 - 3 0 - 3 1 - S e p t 1 + - - 2 + + - 3 + + + 4 + + + + - + + + + - 5 - + - 6 + + + + + - + + -

a . + = w i n d d i r e c t i o n b e t w e e n 1 5 0o a n d 1 7 0 ° ; - = m i s s i n g d a t a .

that the surface w i n d direction of 150° p r o g r e s • at Brownsville again s h o w s a w i n d shift f r o m 150° sively revolves to 240° at 2 0 0 0 m elevation. T h e near t h e surface to 2 4 0 ° at 3 0 0 0 m. S t r o n g winds t e m p e r a t u r e at 2 0 0 0 m w a s 16.7°C, well a b o v e the w e r e observed b e t w e e n 1800 a n d 3 0 0 0 m ranging flight threshold for Heliothis species. f r o m 15 to 22.5 m / s e c . T h e synoptic m a p from M a r c h 2 3 s h o w s strong T h e w in d shift with elevation is a c o m m o n o c c u r • low-level winds (7.5-10 m / s e c ) f r o m south to north r e n c e in south T e x a s in the spring, a n d a s s u m i n g with t h e potential to transport m o t h s 3 5 0 t o 5 0 0 km this is a normal pattern along t h e Gulf C o a s t of overnight a c r o s s southern T e x a s t o w a r d s O k l a • M e x i c o , an aerial transport m e c h a n i s m w o u l d be h o m a a n d Arkansas. T h e p s e u d o - a d i a b a t i c chart available along t h e entire Gulf C o a s t during the

6 5 30

J F M A M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D

Month

Brownsville San Fernando Tampico

Figure 2. Heliothis virescens trap capture at Brownsville, Texas, USA, and San Fernando and Tampico, Tamaulipas, Mexico. Brownsville and San Fernando data are from pheromone traps operated from 1978 through 1980; Tampico data are from light traps operated from 1974 through 1980.

spring to aid the southern migration of a number of 1970, these trap captures at Stoneville occurred on insect species. The wind shift with elevation dis• an average of 33 days prior to the first moth emer• continues in June, and the aerial transport mecha• gence from pupal diapause. Raulston (1979) nism from Mexico along the Gulf Coast would observed a similar asynchrony in diapause emer• appear to break down at this time, with the excep• gence and trap capture for H. virescens in 1978 at tion perhaps of local meteorological events. This is Brownsville, Texas; however, this asynchrony did exemplified in Figure 4, which shows the monthly not occur in 1979 or 1980. It would seem probable average wind direction, speed, and temperature that the moths captured at these various locations taken from pseudo-adiabatic charts from Browns• derive from common source areas. ville, Texas, for June, July, and August 1979. In 1981, Hartstack et al. (1982) observed the The variation in wind direction from June to relationship of H. zea trap capture in pheromone August (18° to 41.8°) below 3000 m is much lower traps at five locations across south Texas and at than noted in the months of March, April, and May Portland, Arkansas, to overwintering emergence at (79° to 124°). Further, the wind direction from Jun e College Station, Texas. Table 3 shows the dates to August tends to be aligned from the coast inland, when trap peaks occurred at these locations as which would decrease the possibility of moth trans• well as at Brownsville, Texas. (Brownsville trap port up the coast of Mexico. As Figure 2 shows, data were supplied by John Norman, Texas Agri• populations are low in northern Mexico during the cultural Extension Service, Weslaco, Texas, and midsummer months, which further decreases the diapause emergence data from Brownsville were probability of major movements at this time of year. supplied by Raulston.). Interestingly, Stadelbacher and Pfrimmer (1972) Initial trap-capture peaks in extreme south o b s e r v e d Heliothis zea adults in light traps at Texas from Brownsville to Corpus Christi, occurred Stoneville, Mississippi, at about the same time trap within a 5-day period from Julian day 79 to 84 captures began to increase in the Lower Rio (Julian day 1 corresponding to 1 January). These Grande Valley of Texas, in mid-March to late trap peaks were synchronized with diapause emer• March. Over a 4-year period, from 1967 through gence at Brownsville, which peaked on day 80.

6 6 Wind speed (m/sec) Temp (o C) 0 5 10 15 3600 0 A 10 20 30 B

3000 High

2400

1800

1200 a - T e m p x - Speed 600 o - Direction

270 360 90 180 270 Wind direction

Wind speed (m/sec) Temp (oC)

0 5 10 15 3600 0 c 10 20 30 0

3000

2400

1800

1200 20.0 a - Temp x - Speed 600 o - Direction

18.8 Low

270 360 96 180 270 Wind direction

Figure 3. Pseudo-adiabatic chart readings and United States synoptic surface weather maps from Brownsville, Texas, for March 17 (A and B) and 23 (C and D) 1980, showing typical weather events for the region during the spring.

6 7 Wind speed (m/sec) T e m p ( ° C )

0 5 10 15 0 5 10 15 0 5 10 15 3 6 0 0 0 10 20 3 0 0 10 20 3 0 0 10 20 30 3000 March A p r i l May

2 4 0 0

1800

a - T e m p 1200 X - S p e e d o-Direction 6 0 0

270 360 90 180 270 360 90 180 270 360 90 180 270

0 5 10 15 0 5 10 15 0 5 10 15 3 6 0 0 0 10 20 30 0 10 20 30 0 10 20 30 3 0 0 0 J u n e July A u g u s t

2 4 0 0

1800

1 2 0 0

6 0 0

270 360 90 180 270 360 90 180 270 360 90 180 270

Wind direction

Figure 4. Average monthly pseudo-adiabatic chart readings from Brownsville, Texas, for the months of March through A ugust 1979, showing typical wind shifts in the spring, which can provide an aerial transport mechanism for moths from the Gulf Coast of Mexico.

Trap-capture peaks occurred progressively later, tures and diapause emergence at the northern moving north and east, with the last peak occurring locations further suggests that these initial peaks at Portland, Arkansas, on day 99. A time difference were derived from the southern locations. The wind of 20 days was observed between trap peaks from flow patterns in south Texas at this time of year, the most southern and northern areas. The peak of (Figs. 3 and 4), also suggest that the Gulf Coast of emergence from diapause at College Station Mexico may be implicated in the production of occurred 22 days after the initial trap peak at that these peaks. Interestingly, 72% of the diapausing location and 39 days after the diapause emer• H. zea pupae we buried at Tampico, Tamaulipas, gence and trap peak observed at Brownsville. Mexico (22°N), emerged between 15 December The synchronization of trap and diapause peaks 1979 and 15 January 1981, and reproductive popu• in extreme south Texas strongly suggests a com• lations of H. zea occur throughout the year at this mon population, and the asynchrony of trap cap• latitude.

6 8 Table 3. Dates of Initial H e l i o t h i s zea trap-capture peaks at six locations in Texas an d Portland, Arkansas, and emergence from diapause peaks at Brownsville and Col lage Station, Texas, 1981.

L o c a t i o n J u l i a n T e x a s A r k a n s a s daya Brownsville Weslaco Raymondville Corpus Christi Coll ege Station Huntsville Portland

7 9 X 8 0 x0b 8 3 X 8 4 X 9 1 X 9 7 X 9 8 X 9 9 X 1 1 9 0 a . Julian day 1 corresponds to 1 January. b . X=trap peak; 0 = diapause emergence peak.

Methods and Needs for Future that used in two of the most exhaustive studies of Research on Heliothis insect migration, involving a number of species in Africa and Australia and the spruce budworm Spp Migration (Choristoneura fumiferana) in Canada. These stu• dies now form the basis for studying migration of Data and references presented in the preceding numerous other insects. Rainey (1974) reviewed section illustrate the mobility of Heliothis spp, a n d the initial work on locust migration and described through inference, their migrating ability. It is evi• the employment of photography, meteorology, and dent, however, that none of these studies has eluci• aviation as well as the biological sciences in the dated an actual migratory movement from one development of methods to track and determine habitat to another, with concomitant ecological stu• the forces instrumental in swarm formation and dies describing these habitats and the insect popu• movement. Later, Rainey (1978) listed as a major lations being supported in them. Hughes (1979) constraint to long-term locust control the period considers the implications of migration in popula• when contact with remnant populations was lost tion dynamics and discusses its relevance in rela• and pointed out that Joyce (1968) suggested main• tion to three major aspects, the first being those taining the needed contact by using aircraft events occurring in Habitat I that elicit migratory equipped with search radar and Doppler radar behavior. These events may be broadly catego• wind-finding equipment. rized as habitat deterioration brought about by mat• Schaefer (1976) reviewed his initial work on uration of host plants, increases in population developing and using radar technology for studying density beyond the carrying capacity of the food insect flight, and provided the framework for a field source, and adverse environmental effects on of radar entomology. In a number of field expedi• either the quality of food or the ability of the orga• tions in Africa, Australia, and Canada, both quantit• nism to reproduce and survive within the habitat. ative and qualitative observations were made on Hughes lists as the second aspect those factors insect flight. These studies provided excellent experienced en route, including intermediate feed• insight into many aspects of insect flight for a ing and/or reproduction sites and environmental number of species, including takeoff, speed, orien• effects, and as a third aspect, the conditions in tation, elevation, and diurnal variations in activity, Habitat II that affect its favorability for reproduction and even revealed detailed structure of wind sys• and survival. tems involved in insect transport. Further, analyses Definitive studies of these events clearly involve of wing-beat frequencies in the echo signature and a vast array of expertise and technology, such as concomitant field observations provided a method

6 9 of insect identification and—under optimum through the use of radar and meteorological tech• conditions—sex differentiation of grasshoppers nology. The radar was located northwest of Tifton, and locusts. Georgia, and was operated by the U.S. Department In one study, Schaefer (1976) was able to of Agriculture. The radar was similar to the one observe radar plumes of Noctuiid moths consisting used in Canada for studying the spruce budworm of H. armigera a n d Spodoptera littoralis arising from (Greenbank et al. 1980). Plumes of insects had a field of groundnut in the Sudan Gezira. He was been observed departing from various groundnut able to observe their takeoff, which peaked about fields in late August of 1981, and one plume was 45 min after sundown, as well as the elevation and detected originating from a sorghum field heavily orientation of the plume. Lingren and Wolf (1982) infested with fall armyworm. observed similar radar plumes arising from cotton Radar observations of insects above the fields near Phoenix, Arizona, which began about 65 sorghum field on 2 September indicated that activ• min after sundown and rose to a height of 300 m. In ity started at 2003 hr and reached a peak at 2012 hr other studies near Phoenix, Wolf (1979) observed (Fig. 5). The plume lasted at least 20 minutes, and insect activity over cotton fields and nearby desert at 2030 hr, significant numbers of insects were areas, and in one instance was able to detect three flying as high as 1000 m above ground. By 2130 hr, layers of insects associated with inversion layers, a a layer of insects had formed at an altitude of 900 phenomenon also reported by Schaefer (1976) and m, and additional insect layers formed later in the Greenbank et al. (1980). night. Greenbank et al. (1980) reviewed 10 years of The higher flying insects originated from fields exhaustive studies on the dispersal of the spruce other than the local sorghum field and were budworm. This long-term investigation incorpo• detected as they passed within radar detection rated the experience of Schaefer, Rainey, and oth• range. No lumping of insect densities was ers, and took a holistic approach to the study of observed as they passed the radar (such as a dispersal. These investigators used eight major cloud of insects from a remote field). Apparently, methods in their studies: observation platforms, the diffusion and mixing of insects from individual night-viewing telescopes, ground-based and air• fields produced a homogeneous flow of insects at borne radar, airborne collecting nets, light traps, the various altitudes. and meteorological equipment including balloon Wind velocities and directions are shown in Fig• releases. With this impressive array of equipment, ure 5. There were variations in wind velocity with observations were made on emigration, moth dis• altitude and with time. At 2058 hr, there was a 150° placement, immigration, and meteorological shift in wind direction. By 0240 hr, a low-level jet events determining or affecting aerial transport. had developed with a maximum velocity of 7.5 The life history status and density of dispersing m/sec at 250 m. moths were also determined as well as the ecologi• Without these types of measurements, estimates cal status of the habitats producing the emigrating of insect displacement must rely on assumptions moths. Fisher and Greenbank (1979) presented a about time and height of insect flight and interpola• population simulation model based upon these stu• tions from synoptic charts as illustrated previously. dies, from which control strategies may be Airflows like the low-level jet shown in Figure 5 adapted. These authors concluded, however, that cannot be interpolated from synoptic charts, and for the spruce budworm, predictive models of dis• insect displacement associated with such an event persal were not feasible, because of the uncontrol• could not be accounted for by using synoptic chart lable meteorological events that determine analysis. Indeed, large errors in displacement esti• direction and distances of movement. mates would occur if only surface wind measure• These studies provide excellent models upon ments were used. which we can base more intensive studies of Helio- Interpretation of radar data is simplified when this dispersal and migration. Indeed, such studies only one insect species is flying, because simple have already been initiated (Lingren et al. 1978, radars do not discriminate between species. When Wolf 1979, Lingren and Wolf 1982, Lingren et al. more than one species is flying, the radar data will 1982), and are currently being expanded. be more meaningful if the radar provides informa• The following radar entomological observations, tion for classifying the targets, as discussed by conducted by W.W. Wolf, illustrate some of the wind Schaefer (1976). A radar that provides polarization, and insect variations that become evident only radar cross section, wing beating, or orientation

7 0 A Speed ( m / s e c )

0 5 10 15 0 5 10 1 5 1200

1000 2058 h 0 2 4 0 h s p e e d s p e e d d i r e c t i o n d i r e c t i o n 8 0 0

6 0 0

400

2 0 0

0 270 360 90 180 270 360 90 180 270

D i r e c t i o n

1200

2 0 1 2 h 2 2 3 0 h 1000 2037 h 0 3 3 0 h 2 1 3 0 h 8 0 0

6 0 0

4 0 0

2 0 0

0 2 4 8 2 4 8 2 4 8 2 4 8 2 4 8 2 4 8 2 4 8 2 4 8 2 4 8 2 4 8

10-2 10-1 10° 101 102 10-2 10-1 10° 101 102 103

Insects/ million m3

Figure 5. Radar observations (2 Sept 1981) of wind profiles (A) and insect densities (B) over a sorghum field near Tifton, Georgia, USA.

information needs to be developed for studying dency on pesticides requires that we develop new multispecies displacements. theories and philosophies for control. Knipling As stated previously, the current impetus in agri• (1978, 1982) provides a theoretical approach to cultural entomology research to reduce our depen• management of Heliothis populations on an area-

71 wide basis. He discusses the relevance of attack• edge the cooperation of Mr. Richard Hagan, Chief ing our Heliothis problems before they become Meteorologist, and assisting personnel of the established as an economic debit in our cropping National Weather Service at Brownsville, Texas, in systems, and advocates the use of combinations of providing the pseudo-adiabatic chart data. suppression methods, such as cultural methods to destroy indigenous reproduction sites; releases of egg and larval parasites; applications of patho• References gens; and autocidal techniques such as the release of sterile, substerile, or hybrid sterile BECKMAN, S.K. 1973. A study of wind-speed maxima insects. near the surface over the south central United States. Such approaches to insect control beyond the M.S. Thesis, Texas A&M University, College Station, Tex, confines of cropping systems per se require a tho• USA. 73 pp. rough knowledge of all aspects of insect population dynamics. Rabb (1978) aptly states that the eco• CALLAHAN, P.S., SPARKS, A.N., SNOW, J.W., and logical definition of populations for management is COPELAND, W.W. 1972. Corn earworm moth: Vertical a major difficulty and must encompass large distribution in nocturnal flight. Environmental Entomology enough geographical areas to account for move• 1: 497-503. ment of the target species as well as its biotic CARPENTER, J.E., SPARKS, A.N., and HARRELL, associates. He further states that suppression tac• E.A. 1982. Effect of temperature on wing beat frequency tics utilizing behavior modifiers, genetic methods, and sustained flight of certain lepidoptera insects. Journal and biotic agents require a wide area approach in of Georgia Entomology (in press). guiding their use. In the context of mobility, popula• tion management then is a problem not only of FISHER, R.A., and GREENBANK, D.O. 1979. A case long-range movement, but also of movement within study of research into insect movement: Spruce budworm the ecosystem, including movement within and in New Brunswick. Pages 220-229 in Movement of highly between managed (crops) and unmanaged host mobile insects: concepts on methodology in research, reservoirs, and movement associated with specific eds. R.L. Rabb and G.G. Kennedy. Raleigh, NC, USA: behavior such as mating, feeding, and host finding. University Graphics. The mobility of the Heliothis species has cer• FRENCH, R.A., and HURST, G.W. 1969. Moth immi• tainly been demonstrated, and the foundations gration in the British Isles in July 1968. Entomologist's have been laid for intensive studies of their move• Gazette 20: 37-44. ment. Further, the importance of studying such movement and its implications in pest manage• GREENBANK, D.O., SCHAEFER, G.W., and RAINEY, ment are recognized. We must now build upon R.C. 1980. Spruce budworm (Lepidoptera: Tortricidae) these foundations to develop the information for moth flight and dispersal: new understanding from can• scientifically sound pest-management systems, opy observations, radar and aircraft. Memoirs of the Ento• and, as Taylor (1979) states, "the scales of time mological Society of Canada 110, Ottawa, Canada. 49 pp. and space needed to produce the sound and con• HAILE, D.G., SNOW, J.W., and YOUNG, J.R. vincing ecological experimentation in flying insect 1975. Movement of adult Heliothis released on St. Croix pests required by agriculture are to be measured in to other islands. Environmental Entomology 4: 225-226. thousands of kilometers and decades—economic entomology like insect ecology must learn to think HARDWICK, D.F. 1965. The corn earworm complex. on these scales of space and time if it is ever to Memoirs of the Entomological Society of Canada 40, increase its impact." Ottawa, Canada. 248 pp.

HARTSTACK, A.W., LOPEZ, J.D., STERLING, W.L., Acknowledgment KING, E.G., MULLER, R.A., and WITZ, J.A. 1982. Long range spring migration of Heliothis zea indi• cated. Environmental Entomology (in press). The authors gratefully acknowledge the efforts of

Dr. R.A. Muller, Professor, Louisiana State Univer• HENDRICKS, D.E., GRAHAM, H.M., and RAULSTON, sity, and State Climatologist, in selecting and pro• J.R. 1973. Dispersal of sterile tobacco budworms from viding explanations of the U.S. synoptic weather release points in northeastern Mexico and southern maps presented in this paper. We also acknowl• Texas. Environmental Entomology 2:1085-1088.

72 HUGHES, R.D. 1979. Movement in population dynam• RAINEY, R.C. 1974. Flight behavior and features of the ics. Pages 14-32 in Movement of highly mobile insects: atmospheric environment. Symposia of the Royal Ento• concepts on methodology in research, eds. R.L. Rabb and mological Society of London 7: 75-112. G.G. Kennedy. Raleigh, NC, USA: University Graphics. RAINEY, R.C. 1978. Possible impact of radar on pest JACKSON, R.D. 1979. Concepts, plans, and current management operations. Pages 81 -86 in Radar, insect research efforts (USDA) in insect migration research for population, ecology, and pest management. NASA Con• insect population management systems. Pages 436-439 ference Publication 2070, Washington DC, USA. in Movement of highly mobile insects: concepts on methodology in research, eds. R.L. Rabb and G.G. RAULSTON, J.R. 1979. Heliothis virescens migration. Kennedy. Raleigh, NC, USA: University Graphics. Pages 412-419 in Movement of highly mobile insects: concepts on methodology in research, eds. R.L. Rabb and JOYCE, R.J.V. 1968. Possible developments in the use G.G. Kennedy. Raleigh, NC, USA: University Graphics. of aircraft and associated equipment. Chemistry and Industry 27 January 1968: 117-120. RAULSTON, J.R., SPARKS, A.N., and LINGREN, P.D. 1980. Design and comparative efficiency of a wind- KNIPLING, E.F. 1978. Eradication of plant pests—Pro. oriented trap for capturing live Heliothis spp. Journal of Bulletin of the Entomological Society of America 24: 44- Economic Entomology 73: 586-589. 52. SCHAEFER, G.W. 1976. Radar observations of insect KNIPLING, E.F. 1982. The rationale for areawide man• flight. Pages 157-196 in Insect flight, ed. R.C. Rainey. agement of Heliolhis populations. Bulletin of the Entomo• London: Blackwell. logical Society of America (in press). SNOW, J.W., and COPELAND, W.W. 1971. Distribution LINGREN, P.D., and WOLF, W.W. 1982. Nocturnal and abundance of the corn earworm in the United States. activity of the tobacco budworm and other insects. In The U.S. Department of Agriculture Plant Pest Control Div• role of biometeorology in integrated pest management, ision, Cooperative Economic Insect Report 21: 71 -76. eds. J.L. Hatfield and I.S. Thomanson. New York, NY, USA: Academic Press. (In press). SNOW, J.W., CANTELO, W.W., and BOWMAN, M.C. 1969. Distribution of the com earworm on St. Croix, U.S. LINGREN, P.D., SPARKS, A.N., RAULSTON, J.R., Virgin Islands and its relation to suppression programs. and WOLF, W.W. 1978. Application for nocturnal studies Journal of Economic Entomology 62: 606-611. of insects. Bulletin of the Entomological Society of Amer• SPARKS, A.N. 1972. Heliothis migration. Pages 15-17 in ica 24: 208-212. Distribution, abundance and control of Heliothis species LINGREN, P.D., RAULSTON, J.R., SPARKS, A.N., in cotton and other host plants. Southern Cooperative and WOLF, W.W. 1982. Insect monitoring technology for Series Bulletin 169, Oklahoma Agricultural Experiment evaluation of suppression via pheromone systems. In Station, Oklahoma State University, Stillwater, Okla, USA. Insect suppression with controlled release pheromone SPARKS, A.N., JACKSON, R.D., and ALLEN, C.L. systems, eds. G. Zweig, A.F. Kydonieus, and M. Beroza. 1975. Corn earworms: capture of adults in light traps on Boca Raton, Florida: CRC Press, (in press). unmanned oil platforms in the Gulf of Mexico. Journal of LOPEZ, J.D. 1976. The role of host phenology in the Economic Entomology 68: 431 -432. population dynamics of the bollworm, Heliolhis zea (Bod- STADELBACHER, E.A., and PFRIMMER, T.R. 1972. die), in the Brazos Valley of Texas. Ph.D. dissertation, Winter survival of the bollworm at Stoneville, Mississippi. Texas A&M University, College Station, Tex, USA. 199 pp. Journal of Economic Entomology 65: 1030-1034.

METCALF, R.L. 1980. Changing role of insecticides in TAYLOR, L.R. 1979. The Rothamsted insect survey - an crop protection. Annual Review of Entomology 25: 219- approach to the theory and practice of synoptic pest 256. forecasting in agriculture. Pages 148-185 in Movement of highly mobile insects: concepts on methodology in PHILLIPS, J.R. 1979. Migration of the bollworm, Heliothis research, eds. R.L. Rabb and G.G. Kennedy. Raleigh, NC, zea (Boddie). Pages 409-411 in Movement of highly USA: University Graphics. mobile insects: concepts on methodology in research, eds. R.L. Rabb and G.G. Kennedy. Raleigh, NC, USA: WOLF, W.W. 1979. Entomological radar studies in the University Graphics. United States. Pages 263-266 in Movement of highly mobile insects: concepts on methodology in research, RABB, R.L. 1978. A sharp focus on insect populations and pest management from a wide-area view. Bulletin of eds. R.L. Rabb and G.G. Kennedy. Raleigh, NC, USA: the Entomological Society of America 24: 55-60. University Graphics.

The Identification and Use of Genetic Markers for Population Dynamics and Control Studies in Heliothis

Alan C. Bartlett and J.R. Raulston*

Abstract

The study of insect population dynamics requires some method of observation of individuals and groups. Some of the best information of this type is obtained through direct observation in the field, but this method is cost- and labor-intensive and requires well-trained and dedicated observers (particularly tor nocturnal species such as Heliothis,). Recently, pheromone trapping has been a great help in assessment of insect numbers in natural populations, but inter• pretation of data from pheromone traps is still uncertain. Insect-marking techniques have long been used to acquire knowledge on insect behavior and dynamics. This paper discusses the use of visible and biochemical genetic markers as tools tor the study of H e l i o t h i s spp population dynamics and reproductive behavior. Body-color and eye-color mutations have great potential tor use as markers, because they are easily re• cognized by workers using pheromone traps or collecting insects by hand in behavior studies. Biochemical markers, such as isozymes, are useful in long-term studies, since they are generally believed to show only minor selective effects in individuals. Procedures for the isolation and purification of mutant strains of Heliothis spp are easily incorporated into any laboratory rearing system if appropriate precautions are taken. The insertion of a genetic marker into the sterile hybrid H. virescens x H. subflexa is given as an illustration of the use of genetic markers in a Heliothis control program.

*U.S. Department of Agriculture, Agricultural Research Service, Western Cotton Research Laboratory, Phoenix, Arizona, and Cotton Insects Research Laboratory, Brownsville, Texas, USA, respectively.

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India 7 5 All modern methods of Heliothis spp management the use of such mutations, and discuss the require economically feasible ways to measure the assumed and actual limitations of genetic markers population density and dynamics of the target pest in Heliothis research programs. species. In fact, integrated pest management (IPM) systems function only if the pest status (population level) can be monitored continuously (Bottrell Mutations Available in 1979). Lingren et al. (1979) stressed the need for Heliothis Spp adequate direct observations of in-field behavior of undisturbed insect populations to determine the In a broad survey of the literature on Lepidoptera base parameters of population density and dynam• genetics, Robinson (1971) listed only DDT resist• ics for pest species under a pheromone control ance as a genetic marker in any Heliothis species. system. That same reasoning is probably also valid However, since the publication of that book, sev• for other suppression techniques. In order to suc• eral mutant characters in Heliothis have been des• cessfully monitor Heliothis population levels, we cribed. Whitten (1973) described a mutant in H. zea must know what the populations would normally do that produces black pupae rather than the normal at a given time (season) under given conditions. In brown pupae of this species. The character is other words, how many Heliothis are out there and inherited as a simple autosomal recessive trait. Th e what are they doing? striking difference in the pupal color of individuals Ideally, we should have a continuous record of homozygous for this mutation could be of value in the whole population of the target species over the studies where larvae or pupae are recovered after critical time period, but time and economics pre• the release of adults (such as in a test on diapause clude such a complete determination. Therefore, induction or host-plant preferences). A yellow- only samples can be taken to provide the clues we eyed variant of the corn earworm was described by require for estimation of the population dynamics of Jones et al. (1977), which was also inherited as an the species. autosomal recessive character. The yellow-eyed One method of studying the behavior, dispersal, mutation also caused a light coloration of the adult migration, or other movement of populations is by body. Some effects of the mutation were noted the use of marked insects of release-recapture when the strain was first isolated, but these effects experiments (Southwood 1978). Several artificial were reported to have disappeared upon outcross• marking techniques (for example, radioisotopes, ing and selection. The behavior of this mutation fluorescent powders, oil-soluble dyes, etc.) have under natural conditions has not been reported, but been used successfully in Lepidoptera to observe since there seems to be no detrimental effect of the gross movements or to identify the released mutation on behavior in the laboratory, this eye- insects. Unfortunately, such artificial markers only color mutant could be used as a population marker last through one generation or less. Artificially a p • in release-recapture studies of H. zea. plied markers do not allow the tracking of a A sex-linked mutant that produces yellow pupae released individual over generations, although rather than the normal brown color was reported by such tracking may be necessary to evaluate such Proshold (1974). This mutation is of great interest factors as generation time, intrinsic rate of since, with proper manipulation of the gene, it cou l d increase, age structure of populations, and sex be used for sexing large numbers of this species for ratio changes over time. This paper discusses the control purposes. The distribution of sex-linked loci use of visible and biochemical mutations to permit in Lepidoptera (Fig. 1) is discussed later in this tracking of released individuals over time and gen• paper in relation to insecticide resistance. The erations after release. combination of a sex-linked visible marker with The recovery and use of genetic markers in stu• sex-linked resistance loci would be valuable in the dies of insect population dynamics has been dis• development of genetic sexing techniques as well cussed for several species by Bartlett (1967, as for use in release-recapture experiments. 1981 b), Stock (1979), and Huettel (1979). How• Sluss et al. (1978a, 1978b) compared isozyme ever, the use of genetic markers in Heliothis control differences between H. virescens a n d H. zea. In programs or biological studies has not previously addition to demonstrating the value of isozyme stu• been examined. Therefore, this paper will demon• dies to differentiate these two species, these strate methods for recovery of visible and bio• authors also showed that much genetic variation chemical mutations in Heliothis species, illustrate exists within a species and that this variation cou l d

76 S u s c e p t i b l e (S)

R e s i s t a n t (R) 9 0 R x S

S x R 80

7 0

6 0

0 . 1 0 . 2 5 0 . 5 1 2 . 5 5 10 2 5 50 100

D o s e c o n c e n t r a t i o n ( l o g )

Figure 1. Response of susceptible (S) and resistant (R) strains of Heliothis virescens and the reciprocal F1 crosses between them to doses of methyl parathion applied to larvae (data from Wolfenbarger et al. 1981).

be u s e d as genetic markers in biological experi• Heliothis species, long-term studies of migration ments. For example, the hexokinase (HEX-A) should be highly productive. e n z y m e s y s t e m in H. vlrescens has four alleles in T h r e e visible mutants of H. virescens have b e e n the population studied by Sluss et al. (1978b), but isolated a n d are maintained by J.R. Raulston another population of H. virescens c o n t a i n e d only (unpublished data). O n e strain has a dominan t three alleles at the s a m e locus. If s u c h g e n e fre• body-color mutation w h i c h has great potential as a q u e n c y variations w e r e e x a m i n e d over t h e g e o g r a • marker as well as for control programs in this s p e • phic range of any Heliothis species a n d e x t e n d e d cies. T h e other two strains carry recessive a u t o • to a n u m b e r of different loci (as is easily d o n e with somal mutations w h i c h also have potential as isozyme analyses), o n e may follow the migration markers in release-recapture experiments. T h e patterns of t h e s e ubiquitous species. Sell et al. utilization of these markers is d i s c u s s e d in a later (1974a, 1974b) d e s c r i b e d a n d analyzed a polymor• section of this paper. phic e s t e r a s e (EST-ll) s y s t e m in H. zea a n d out• T h e final type of genetic markers available in lined t h e utility of s u c h a s y s t e m in st ud yin g t h e Heliothis s p e c i e s a r e t h o s e f o u n d in t h e dispersal of this species. S i n c e isozymes a r e g e n • insecticide-resistant strains present in many labor• erally r e g a r d e d as transparent to selective pres• atories a n d in fields around the world. Not m a n y of sures, a n d g e o g r a p h i c variations a p p e a r to be these resistant strains have b e e n e x a m i n e d in present in most insect s p e c i e s a n d particularly in e n o u g h detail to m a k e t h e m useful as genetic

77 markers, but if their potential w e r e realized, per• T h e r e are probably other interesting genetic h a p s m o r e genetic analyses w o u l d be c a r r i e d out. marker s t o c k s available in laboratories a r o u n d t h e W o l f e n b a r g er et al. (1981) studied methyl parathion world that h a v e not b e e n p l a c e d in t h e literature resistance in H. virescens to discover t h e genetic b e c a u s e t h e potential for their use is not a p p r e • nature of the resistance. In c r o s s e s b e t w e e n s u s • ciated. In addition, there are simple w a y s to obtain ceptible a n d resistant strains, Wolfenbarger et al. n e w genetic markers that have not b e e n e m p l o y e d (1981) f o u n d that w h e n resistant m a l e s w e r e in Heliothis species. T h e remainder of this paper

c r o s s e d to susceptible females, t h e F1 progeny e x a m i n e s both the acquisition a n d utilization of w e r e m o r e resistant t h a n progeny of the reciprocal s u c h genetic m a r k e r s in Heliothis r e s e a r c h c r o s s (Fig. 1). T h i s result is typical of at least partial programs. sex-linked inheritance of the gene or genes that control t h e r e s p o n s e of this strain to insecticide e x p o s u r e . Figure 2 d i a g r a m s t h e expectations in L e p i d o p t e r a for a sex-linked resistance g e n e (R). Isolation and Maintenance T h e distribution of g e n o t y p e s in m a l e s a n d females s h o w s that males c a n be h o m o z y g o u s RR, h o m o z • of Mutations y g o u s rr, or heterozygous (Rr), but f e m a l e s c a n carry only o n e of t h e alleles, either R or r, but not M a n y investigators have o b s e r v e d aberrant indi• both, if t h e trait is sex-linked. T h e e x i s t e n c e of a viduals in Heliothis colonies, but for lack of time or s e x - l i n k e d resistance l o c u s in H. virescens has expertise, h a v e duly noted but promptly d i s c a r d e d several possibilities for use in population d y n a m i c s these aberrant individuals. Laboratory cultures are studies a n d in control programs. the best a n d most readily available s o u r c e of mutant genes. O f t e n a t h o r o u g h e x a m i n a t i on of individuals in a laboratory culture will reveal the p r e s e n c e of aberrants, w h i c h should be bred sys• tematically to reveal whether the c h a r a c t e r is Lepidoptera sex linkage inherited. All stages of t h e life c y c l e must be e x a m • ined, s i n c e mutations c a n affect any stage of devel• o p m e n t (Bartlett 1981 b). T a b l e 1 lists s o m e mutant c h a r a c t e r s that have b e e n f o u n d in e c o n o m i c spe• F e m a l e M a l e cies of Lepidoptera. If an existing laboratory population does not r r R s h o w any morphological variation in a preliminary P1 X Y X X X r e s i s t a n t susceptible e x a m i n a t i on of a high proportion of t h e population, t h e n the next step is to inbreed t h e population to r e x p o s e any recessive mutations that m a y be car• X Y x R x r F1 ried by t h e colony. M o s t entomologists c o n s c i e n • susceptible r e s i s t a n t tiously a v o i d inbreeding of their insect colonies, s i n c e it is c o n s i d e r e d to be detrimental; however, R e c i p r o c a l cross inbreeding is n e c e s s a r y to e x p o s e recessive m u t a • tions. S i n c e only a s a m p l e of t h e population is s u b j e c t e d to the process, no p e r m a n e n t h a r m is X r Y X X R X R P1 d o n e to t h e colony. O n c e a mutation is isolated a n d susceptible r e s i s t a n t purified, heterozygosity may be r e c o v e r e d in the mutant strain. An effective inbreeding s c h e m e is X R Y X R X r g i v e n in Bartlett (1981b): (1) A n u m b e r of single- F1 r e s i s t a n t r e s i s t a n t pair c r o s s e s are m a d e b e t w e e n individuals from a r a n d o m - m a t i n g laboratory population. (2) F r o m

Figure 2. Inheritance of sex chromosomes and e a c h single-pair cross m a d e in t h e parental gener- tion, the F1 p r o g e n y are m a s s - c r o s s e d to p r o d u c e types of F1 progeny resulting from reciprocal an F2 population. If a recessiv e mutation w e r e p r e s • crosses of P1 individuals carrying a sex-linked locus for resistance to an insecticide. R=allele ent in either of t h e original parents, t h e n o n e - for resistance; r = allele for susceptibility to the sixteenth of the F2 p r o g e n y will be e x p e c t e d to s h o w insecticide. (Source: Wolfenbarger et al. 1981.) t h e mutant phenotype. Obviously, o n e must e x a m -

7 8 Table 1. Types of mutant characters observed In differe n t s p e c i e s o f L e p i d o p t e r a .a

C h a r a c t e r S p e c i e s Inheritanceb

E y e c o l o r Bomby x mori D, r, a, s Pectinophora gossypiella r, a , s Sitotroga cerealella r, a Cadra cautella r, a Sterrha seriata r, a

Larval color B. mori D , r, a S. seriata r, a P. gossypiella r, a Ostrinia nubilalis r, a Celerio euphorbiae r, a

Pupal color Heliothis zea r, a B. mori D , r, a

E g g c o l o r B. mori D, r, a, s

E g g s h a p e B. mori D, r, a, s

Wing color, pattern, or shape C. cautella r, a P. gossypiella D , r, a H. virescens D . r, a Pieris protodice r. a S. seriata D , r, a B. mori D , r, a Papilio dardanus D , a

B o d y c o l o r o r p a t t e r n B. mori D , r, a , s P. gossypiella D , r, a S. seriata D , r, a P. dardanus D , r, a H. virescens D , r, a

S e x o r g a n c o l o r B. mori D , r, a P. gossypiella r, a S. seriata r, a

Larval size B. mori r, a

D i a p a u s e o r v o l t i n e c h a n g e B. mori r, a P. gossypiella D , a , s a . This list is not intended to be exhaustive, only to su ggest characters that can be altered by mutations. References are omitted to conserve space, b u t m a n y c a n b e f o u n d i n R o b i n s o n ( 1 9 7 1 ) o r o b t a i n e d f r o m t h e a u t h o r s . b. D = dominant or codominant, r = recessive, a = autosom a l , s = s e x - l i n k e d .

ine more than 16 individuals to expect to find the normal-appearing siblings are mass-crossed to mutant. If no aberrant individuals are found in 50 to produce F3 progeny. Mutants will again appear in

75 progeny in an F2 family, it is reasonable to the F3 and can be added to the pure culture started assume that the family does not contain a visible in the F2 generation. (4) This inbreeding process is mutation and it may be discarded. (3) If any visible continued until the pure colony has sufficient aberrations are found, then the family is kept for numbers to sustain the population. (5) At this point, further breeding. The mutants are made into a pure if any detrimental effects of inbreeding are appar• culture (that is, a mutant X mutant cross), while ent in the mutant colony, an outbreeding scheme

7 9 c a n be initiated to increase heterozygosity in the b e t w e e n t h e original m a r k e d insects a n d native genetic b a c k g r o u n d of t h e p u r e culture. insects. In t h e third generation after the original T h e n u m b e r of parental c r o s s e s to be m a d e will release, t h e investigator w o u l d be able to identify d e p e n d partly u p o n t h e r e s o u r c e s available to the three types of individuals: (1) heterozygous investigator. A f e w calculations will estimate the mutants resulting f r o m c r o s s e s b e t w e e n natives

expectations for recovery of a mutant culture f r o m a n d either released h o m o z y g o t e s or F1 heterozy- a r a n d o m - m a t i n g population. T h e g e n o m e of Helio- gotes, (2) h o m o z y g o u s mutants resulting from this species contains 31 (2n=62) pairs of c h r o m o - c r o s s e s b e t w e e n the released h o m o z y g o t e s a n d

s o m e s ( C h e n a n d G r a v e s 1970); thus a single-pair the F1 heterozygotes or a m o n g R heterozygotes, c r o s s will s a m p l e 1 2 4 c h r o m o s o m e s . If e a c h a n d (3) native x native crosses. T h u s , with a c h r o m o s o m e contains, on the average, 1000 loci c o d o m i n a n t mutation, there is a possibility of study• (Hartl 1977), t h e n e a c h single-pair cross is s a m • ing mating interactions b e t w e e n native a n d pling about 124 0 0 0 loci. If t h e s p o n t a n e o u s m u t a • released individuals a c r o s s three generations in tion rate is, as e s t i m a t e d in other organisms, about t h e field without the heavy d e m a n d s of time a n d 1 X 10- 6 per locus (Ayala 1976), t h e n o n e single- m o n e y i m p o s e d by direct observation of mating pair mating w o u l d be e x p e c t e d to yield about 0.1 pairs. newly arisen mutation. T e n matings, therefore, O n c e a mutant culture is established in the labor• s h o u l d p r o d u c e about o n e n e w mutation. S i n c e atory, it is n e c e s s a r y to keep it h o m o z y g o u s for the s o m e of t h e s e mutations will not be visible (that is, mutant g e n e a n d vigorous. T o m a n y biologists, they will be b i o c h e m i c a l or affecting internal struc• t h e s e are o p p o s i n g c o n c e p t s . This view results tures), we m a y a s s u m e that t h e yield of n e w visible f r o m t h e almost universal recognition of t h e detri• mutations will be less t h a n 0.1 per mating. Even if mental effects of inbreeding on a n i m a l vigor a n d we a s s u m e that only 1 0 % of the n e w mutations are reproduction. However, c h a n g e s in the size of visible, we c o u l d e x p e c t o n e visible mutant from inbreeding coefficients d e p e n d wholly on the size 100 single-pair crosses. Of course, mutations of t h e population being bred in t h e laboratory, as c o u l d have o c c u r r e d in earlier generations of labor• s h o w n by the following formula (Falconer 1960) for atory rearing a n d s h o u l d also be present in the c h a n g e i n t h e i n b r e e d i n g c o e f f i c i e n t o v e r population, thus increasing the probability of a vis• generations: ible mutant. ΔF = 1 /8Nm + 1 / 8 N t S i m p l e M e n d e l i a n mutations s h o w only three w h e r e F = the inbreeding coefficient, Nm = the t y p e s of inheritance: recessive, dominant, or n u m b e r of males in t h e breeding population, a n d Nf c o d o m i n a n t . If a mutant allele s h o w s its p h e n o t y p e = t h e n u m b e r of females in the breeding population. only w h e n t w o identical alleles are present in an If equal n u m b e r s of males a n d females w e r e individual, then t h e trait is said to be recessive; if u s e d to p r o d u c e progeny, the c h a n g e in inbreeding only o n e allele is n e e d e d for full expression of the coefficients per generation for Nm = Nt = 1 0 , 1 0 0 , or mutant trait, t h e n the trait is said to be inherited as a 1 0 0 0 w o u l d be 0.025, 0.0025, or 0.00025. T h u s it dominant; if an individual s h o w s o n e a p p e a r a n c e a p p e a r s that inbreeding i n c r e a s e s very slowly as w h e n heterozygous a n d a different a p p e a r a n c e population size e x c e e d s 100 pairs of breeding indi• w h e n h o m o z y g o u s , the trait is inherited as a viduals. Very few laboratory populations are m a i n • codominant (or intermediately dominant) trait. Most tained at n u m b e r s less than 100 pairs, especially if newly arisen visible mutations are recessive. a population is to be used for release. T h e problem D o m i n a n t a n d c o d o m i n a n t visible mutants are with inbreeding arises in the first few generations t h e easiest c l a s s e s of mutant to detect, but the after isolation of t h e mutation, w h e n n u m b e r s of least frequent in o c c u r r e n c e . T h e y are also the mutant individuals are low. In a study of t h e effects most valuable mutations to use in release- of inbreeding on reproduction a n d viability in Hyle- r e c a p t u r e experiments s i n c e not only will the mya antiqua during t h e isolation of h o m o z y g o u s released individuals be m a r k e d , but any progeny of translocation stocks, Robinson (1977) f o u n d w i d e m a t i n g s with t h e released individuals will also be differences in r e s p o n s e of various lines to t h e m a r k e d . C o d o m i n a n t mutations are extremely v a l • effects of inbreeding. In five of t h e inbred lines there uable in this t y p e of experiment, s i n c e o n e c o u l d w a s a significant reduction in e g g hatchability, but theoretically release m a r k e d individuals of o n e sex in three other lines no s u c h reduction w a s for t w o generations a n d still be able to tell the o b s e r v e d . No effect of inbreeding on mating pro•

released individuals from the F1 p r o g e n y of matings pensity or sex ratio w a s o b s e r v e d in any of the lines

8 0 over three generations of intensive inbreeding Use of Visible Genetic Markers (Robinson 1977). Similar results have b e e n o b s e r v e d in Aedes aegypti (Craig a n d H i c k e y An effective marking t e c h n i q u e for insect r e s e a r c h 1967) a n d Drosophila melanogaster (Lints 1961). should meet the following m i n i m u m criteria: Typically, fitness does d e c l i n e in inbred lines for a • e a s e of application of the marker; few generations; s o m e lines are lost, but then sur• • minimal manipulation of insects to apply the viving lines are easily maintained, a n d it a p p e a r s marker; that inbreeding depression should not be a serious • e a s e of recognition of the marker by laboratory obstacle to the production of mutant stocks of or field personnel; insects (Robinson 1977). • certainty of persistence of the marker through If inbreeding depression does o c c u r in Heliothis the life stages of the organism; species a n d a g o o d mutant stock is h a m p e r e d by • relative freedom from deleterious biological poor reproduction or viability, it is possible to out- effects d u e to the marker. breed the strain to an unrelated population a n d Visible genetic markers m e e t these criteria very t h e n to re-isolate the mutant culture. This p r o c e • well; however, previous work using visible genetic dure will take t w o generations to recover homozy• markers has been s u b j e c t e d to the criticism that, g o u s mutants. If the breeding populations are kept b e c a u s e natural selection operates on these large e n o u g h , t h e n t h e c h a n g e in inbreeding coeffi- markers, they do not meet the last criterion (Huettel cient c a n be kept low, as s h o w n by the previous 1979). In most studies of population d y n a m i c s , the formula for ΔF. T h e strain used for outbreeding genetic markers should not be e x p e c t e d to persist should not be the s a m e strain used to p r o d u c e the more than t w o or three generations. If the markers mutant in the first place, s i n c e t h e mutant strain will u s e d in release-recapture experiments are c h o s e n already contain loci in c o m m o n with that strain. To carefully a n d adequate preliminary investigations maximize heterozygosity in the re-isolated mutant m a d e to determine the extent of deficiencies, t h e n strain, o n e should use either a newly colonized wild this factor should not seriously inhibit the use of strain or a strain colonized in another laboratory. visible genetic markers in Heliothis research. T h e m a i n t e n a n c e of mutant strains of Heliothis is T h e successful use of visible genetic markers in no m o r e difficult t h a n the m a i n t e n a n c e of any c o l • the boll weevil, c a b b a g e looper, and pink bollworm onized strain (nor is it any easier!). Certain p r e c a u • has recently been d i s c u s s e d by Bartlett (1981 b). tions c o m m o n to all rearing p r o c e d u r e s should be T h e markers in e a c h c a s e were melanic body- e m p h a s i z e d . First, population levels s h o u l d be kept color mutations. T h e s e mutations are often inher• as high as possible to avoid inbreeding problems. ited as dominant or codominant characters, and, S e c o n d , genetic purity of the strain must be m a i n • judging by the s u c c e s s of melanic forms in L e p i - tained so that w h e n releases of the mutant culture doptera native to industrial areas (Ford 1964), often are m a d e the experimenter is sure that c a p t u r e d have little detrimental effect on the carrier. wild (native) individuals are not part of the released To illustrate the use of a visible melanic genetic population. (If s o m e wild-type individuals are pres• marker in a Heliothis control p r o g r a m , we h a v e ent in the release strain, then that proportion must c h o s e n to e x a m i n e the marker, black body, in Heli• be accurately measured). Mutant strains of insects othis virescens (Raulston, unpublished). This r e s p o n d to quality control in rearing just as other mutation c a u s e s t w o significant, a n d easily laboratory stocks do. T h e quality of a laboratory- observed, c h a n g e s in the body color of the insect. reared strain of insects d e p e n d s a great deal on the In the b l a c k - b o d y mutant, wing color is c h a n g e d to purpose for w h i c h it is intended. In this discussion, a dark green, wifh no e v i d e n c e of t h e normal strip• b e c a u s e the prime p u r p o s e of the mutant strain is ing pattern. T h e a b d o m e n a n d thorax of this mutant to interact as normally as possible with t h e native are a dusky black rather t h a n the normal light grey insects, the experimenter must keep the colonized or c r e a m y white color. This mutation is inherited as strain as nearly like the field strain as possible. T h e a dominant character with recessive lethal effects; effects of laboratory rearing on the behavior a n d its inheritance pattern is s h o w n in Figure 3a. An usefulness of insect species h a v e been d i s c u s s e d individual carrying two of t h e alleles controlling recently (Boiler 1979; Huettel 1979; Bartlett 1981 a). black body color will die, but an individual carrying T h e s e publications should be c o n s u l t e d for only o n e allele for black body color has t h e typical detailed a d v i c e on t h e genetic effects of laboratory mutant phenotype. T h e use of a similar body-color rearing. mutation in t h e c a b b a g e looper (Trichoplusia ni) for

81 3 a body locus. However, since production of the B / + X + / + hybrid strain involves continuous outcrossing of P1 B l a c k W i l d t y p e the hybrid females to normal males, no added work is involved in the maintenance of the black-body 1 hybrid strain. In the hybrid black-body strain, about

1 / 2 B / + 1 / 2 + / + 66% of the F1 progeny will have the black-body F1 B l a c k W i l d t y p e marker. When this strain is released in an autocidal control program, it has several advantages over an unmarked or mechanically marked release strain. B / + X B / + P1 First, over two-thirds of the released individuals B l a c k B l a c k carry the black body color and can be recognized 2 in recapture studies. If selection is practiced on the strain before release (that is, if the wild-type individ• 1/4 B/B 2/4 B/+ 1/4+/ + F1 uals are removed), then all of the released individu• D i e B l a c k W i l d t y p e als would be marked. As the released females mate 3 b and reproduce in the field, 50% of their progeny will carry the black marker, and the success of the P B l a c k male X Hybrid female 1 release program can be evaluated in the first gen• females: 1/2 black, 1/2 wild type eration and subsequent generations simply by F1 males: 1/2 black, 1/2 wild type (sterile) counting the number of black individuals captured versus the number of native individuals captured. F a n d l a t e r F 2 At present, the evaluation of the success of this sterile hybrid release program depends upon the P r o g e n y d i s t r i b u t i o n a s i n capture and subsequent testing of sterility of live cross (1) or (2) above (depending on male encountered) males from the release zone. Such sterility testing is a costly and time-consuming process compared Figure 3. (a) Crosses showing the distribution to the simple counting of mutant individuals in a of progeny from a mating of an individual carry• pheromone trap. ing the black body color mutation of H. vires• In addition to simplifying evaluation of the hybrid c e n s . The same distribution is found regardless release program, the recessive lethal locus gives of sex carrying the trait, (b) Distribution of pro• an added dimension of protection against the geny when a hybrid female (F1 or backcross breakdown of hybrid sterility. If some of the cross e s progeny of H. virescens x H. subflexa cross) is between hybrid females and native males pro• crossed to a black-body male. duced fertile male progeny, then 50% of those males would carry the black-body gene. These an autocidal control program was described by males crossing with subsequently released Bartlett and Butler (1975). Thus this body-color females would then produce 25% lethality in the mutation shows promise as a control tool simply progeny due to the presence of two black-body because of the nature of the inheritance of the genes in the progeny. Furthermore, these black- g e n e . body males could be collected and tested for steril• However, because of the existence of sterility in ity periodically. The magnitude of this work would H. virescens a n d H. subllexa hybrids (Laster 1972), be reduced from testing all males (in the case of an this mutant offers even further promise. In Figure unmarked release program) to testing only those 3b, a series of crosses are diagrammed to illustrate males that the experimenter knew were progeny of the incorporation of this mutant into the hybrid. Only released hybrid females. females of the hybrid strain are fertile; thus black- Previously we mentioned that two recessive body H. virescens males must be used to insert the body-color mutations (striped body and veined mutant gene into the hybrid strain. Black-body wing) of H. virescens are available (Raulston, females are selected from the Ft progeny of the unpublished). Although recessive mutations can• cross between hybrid females and black-body not be conveniently followed over generations in males and crossed again to males of the black- the field, they are still excellent tools for population body strain. The strain will never be pure-breeding, assessment at given points in time. The investiga• because of the recessive lethal nature of the black- tor should observe certain precautions: (1) A

82 preliminary estimate of population densities should control schemes. If females from a strain homozy• be made to determine if sufficient numbers of the gous for the resistance gene were crossed to marker will be available to produce enough insects males carrying the susceptible allele at that locus, for recapture. (2) Releases should be made during all F1 males would be resistant to the chemical, but the inactive period of the species (for Heliothis spp all females would be susceptible (Fig. 2). The dis• this means daylight releases). (3) Releases should criminating dose applied to the F1 progeny would be made over a short period of time (1 or 2 days kill the females and preserve the males for further only) to provide an estimate of survival rates. (4) use (for example in a sterile-male release pro• Releases must be scattered over the complete gram). This type of automatic (or genetic) sexing range of the recapture area so that complete mix• has been used successfully in mosquitoes, but has ing of released and native insects can take place, not yet been used in Heliothis species. or alternatively, if movement of the released insects is of interest, then one point of release should be Use of Isozyme Markers chosen, and intensive trapping or collection should be made at points radiating out from the release A number of review articles have been published point in a precise array. In either case, records from that explain the methods of electrophoresis used to various parts of the recapture area must be exam• identify isozyme markers and the use of those ined individually for differences in numbers of markers in population dynamics studies of insects recaptured insects which may be dependent on the (Pashley and Bush 1979; Steiner and Joslyn 1979; movement of the released individuals or variation in Stock 1979; Huettel 1979). The presence of iso• density of the native population over the habitat z y m e variants in Heliothis species has been m e n • (Southwood 1978). tioned previously. A desirable feature of isozyme The use of genetic markers must be subjected to genetics lies in the ease with which an experimen• the same care and interpretation as any other ter can obtain genetic variation. Individual insects marking method. The advantages of these markers can be examined for as many as 30 isozyme loci, are in the ease of use and permanence of the and up to 70% of these loci may show polymor• marker, not only over the life of the individual, but phisms. Many investigators prefer these "invisible" over generations of the species. markers in release-recapture experiments b e c a u s e they do not affect fitness appreciably or alter normal behavior, since most variant alleles Use of Insecticide are already present in the population. In fact, one of Resistance Genes the limitations of this m e t h o d is that there is so m u c h variation present in most populations that it is Certain strains of H. virescens seem to possess a hard to find loci that will discriminate between pop • sex-linked methyl parathion resistance allele (Wol- ulations without a great deal of experimentation. fenbarger et al. 1981). If strains containing such an However, in ubiquitous Heliothis s p e c i e s there is a allele could be purified (this has not yet been good chance that populations will differ in rare attempted in Heliothis species), then it would be alleles at various loci, which can serve as popula• possible to use the strain not only as a marker tion markers. stock, but in t h e d e v e l o p m e n t of specific control programs as well. Young (1979) used patterns of insecticide resistance of the fall armyworm to three Conclusions insecticides to determine the possible origins of this insect in the eastern United States during 1977. The use of artificial markers for studying insect A similar study could be done in a more elegant population dynamics and reproductive behavior is manner if one knew the inheritance pattern of the well accepted. However, many artificial markers, insecticide resistance. A strain homozygous for a such as dyes, radioactive materials, and mutilation sex-linked resistance gene would also permit inter• are difficult to apply, affect the behavior of the esting combinations of release and treatment to m a r k e d insects, a n d / o r last for only a short time change sex-ratios or otherwise manipulate the during the insect's life cycle. The use of either target population. visible or biochemical genetic markers could help A sex-linked resistance marker would also be investigators to avoid many or all of these helpful in the development of various autocidal problems.

8 3 Good visible mutants have been reported in HARTL, D.L. 1977. Our uncertain heritage: genetics and s o m e Heliothis spp, but none of these mutations human diversity. Philadelphia, USA: Lippincott. 494 pp.

are presently in use as markers in behavioral or HUETTEL, M.D. 1979. G e n e t i c a p p r o a c h e s t o b a s i c release programs, probably because very little problems in insect behavior and ecology. Pages 161 -1 6 9 research has been done on the biological charac• in Genetics in relation to insect management, eds. M.A. teristics of these mutants. Further research must Hoy and J.J, McKelvey. New York, USA: The Rockefelle r be done to help demonstrate the usefulness of Foundation. genetic markers in behavioral studies and control JONES, R.L., WIDSTROM, N.W., and PERKINS, D. programs as well as to isolate valuable mutations in 1 9 7 7 . Yellow-eye variant of the corn earworm. Journal of s p e c i e s s u c h as H. armigera, where no mutations Heredity 68: 264-265. are now available. LASTER, M.L. 1972. Interspecific hybridization of Helio- this virescens a n d H. subflexa. Environmental Entomol- o g y 1 : 6 8 2 - 6 8 7 .

LINGREN, P.D., RAULSTON, J.R., SPARKS, A.N., References and PROSHOLD, F.I. 1979. Tobacco budworm: noctur• nal behavior of laboratory-reared irradiated and native AYALA, F.J. 1976. Molecular genetics and evolution. adults in the field. USDA ARR-W-5, February, U.S. De p a r t • Pages 1 -20 in Molecular evolution, ed, F.J. Ayala. S u n d e r • ment of Agriculture, Berkeley, Calif, USA. 17 pp. land, Maryland: Sinauer Associates. LINTS, F.A. 1961. D i v e r s i t y by i n b r e e d i n g in Drosophila BARTLETT, A.C. 1967. G e n e t i c m a r k e r s i n t h e boll melanogaster. Genetica 32: 177-199. weevil. Journal of Heredity 58: 159-163. PASHLEY, D.P., and BUSH, G.L. 1979. The use of BARTLETT, A.C., and BUTLER, G.D., Jr. allozymes in studying insect movement with special refer• 1 9 7 5 . Genetic control of the cabbage looper by a reces• ence to the codling moth, Laspeyresia pomonella (L.) sive lethal mutation. Journal of Economic Entomology 6 8 : (Olethreutidae). Pages 333-341 in Movement of highly 331 - 3 3 5 . mobile insects: concepts and methodology in research, BARTLETT, A.C. 1981a. Genetic processes of domes• eds. R.L Rabb and G.G Kennedy. Raleigh, NC, USA: t i c a t i o n . i n Advances and challenges in insect rearing, U n i v e r s i t y G r a p h i c s . eds. E.G. King and N.C. Leppla. U.S. Department of A g r i • PROSHOLD, F.I. 1974. A yellow pupal body, sex-linked culture Handbook. (In press.) mutant in the tobacco budworm, Heliothis virescens BARTLETT, A.C. 1981b. Genetic markers, discovery (Lepidoptera: Noctuidae). Canadian Entomology 106: and use in insect population dynamics studies and con • 1 1 9 5 - 1 2 0 0 . trol programs. In International Symposium on the Sterile ROBINSON, A.S. 1977. G e n e t i c c o n t r o l o f Hylemya Insect Technique and the Use of Radiation in Geneti c antiqua. II. Can inbreeding depression be a serious obsta• Insect Control, Vienna, Austria. IAEA-SM-255. (In press.) cle to the development of homozygous rearrangement BOLLER, E.F. 1979. Behavioral aspects of quality in lines? Entomologia Experimental et Applicata 21: 20 7 - insectary production. Pages 153-160 in G e n e t i c s in r e l a • 2 1 6 . tion to insect management, eds. M.A. Hoy and J.J. Mc K e l - ROBINSON, R. 1971. Lepidoptera genetics. New York, vey. New York, USA: The Rockefeller Foundation. USA: Pergamon Press. 687 pp. BOTTRELL, D.R. 1979. Integrated pest management. SELL, D.K., WHITT, G.S., and LEE, L.K. 1974a. Inherit• Washington, DC, USA: U.S. Government Printing Offic e . ance of est-lI phenotypes in the corn earworm. Journ a l o f 1 2 0 pp. Heredity 65: 243-244. CHEN, G.T., and GRAVES, J.B. 1970. Spermatogene• SELL, D.K., WHITT, G.S., METCALF, R.L., and LEE, sis of the tobacco budworm. Annals of the Entomologic a l L.K. 1974b. Enzyme polymorphism in the corn earworm, Society of America 63: 1095-1104. Heliothis zea (Lepidoptera: Noctuidae). Hemolymph este• CRAIG, G.B., and HICKEY, W.A. 1967. G e n e t i c s o f rase polymorphism. Canadian Entomologist 106: 701- Aedes aegypti. P a g e s 6 7 - 1 3 1 in Genetics of insect vec• 7 9 0 . tors of disease, eds. S.W. Wright and R. Pal. New Yo r k , SLUSS, T.P., SLUSS, E.S., GRAHAM, H.M., and USA: Elsevier Press. 794 pp. DUBOIS, M. 1978a. Allozyme differences between Heli• FALCONER, D.S. 1960. Introduction to quantitative othis virescens a n d H. zea. Annals of the Entomological genetics. New York, USA: The Ronald Press. 365 pp. Society of America 71: 191 -195.

FORD, E.B. 1964. Ecological genetics. London, UK: SLUSS, T.P., ROCKWOOD-SLUSS, E.S., PATANA, Methuen. 335 pp. R., and GRAHAM, H.M. 1978b. Dietary influenced allo-

8 4 zyme differences between laboratory populations of Heli- othis virescens. Annals of the Entomological Society of America 7 1 : 367-371.

SOUTHWOOD, T.R.E. 1978. Ecological methods. Lon• don, UK: Chapman and Hall. 524 pp.

STEINER, W.W.M., and JOSLYN, D.J. 1979. Electro- phoretic techniques for the genetic study of mosquitoes. Mosquito News 39: 35-54.

STOCK, M.W. 1979. Genetic markers in applied research on forest Lepidoptera. Pages 328-332 in Move• ment of highly mobile insects: concepts and methodology in research, eds. R.L. Rabb and G.G. Kennedy. Raleigh, NC, USA: University Graphics.

WHITTEN, C.J. 1973. Inheritance of a genetic marker in the tobacco budworm. Annals of the Entomological Society of America 66: 1219-1220.

WOLFENBARGER, DA., RAULSTON, JR., BART- LETT, A.C., DONALDSON, G.E., and LOPEZ, P.P. 1981. Tobacco budworm: selection for resistance to methyl parathion from a field-collected strain. Journal of Economic Entomology 74. (In press.)

YOUNG, J.R. 1979. Assessing the movement of the fall armyworm (Spodoptera frugiperda) using insecticide res• istance and wind patterns. Pages 344-351 in Movement of highly mobile insects: concepts and methodology in research, eds. R.L. Rabb and G.G. Kennedy. Raleigh, NC, USA: University Graphics.

8 5

Distribution of Heliothis armigera Eggs on Cotton in the Sudan Gezira: Spatial and Temporal Changes and their Possible Relation to Weather

Margaret J. Haggis*

Abstract

To determine the extent to which the distribution of ovipositing H e l i o t h i s armigera might be "clumpy" rather than random, the numbers of eggs during September-October, the first half of the cotton-growing season throughout the Sudan Gezira, were subjected to analyses of variance. It was found that at any time there was more variability between than within areas, highly significantly so for units of 600 to 700 km2. Within all areas, the numbers of eggs varied very significantly with time, and manyfold increases in numbers of eggs occurred Simultaneously over thousands of square kilometers. In every 3-day period there were two or more significantly different levels of infestation, each extending over areas ranging from a few hundred to several thousand square kilometers; the boundaries of such areas changed continually, and no consistent differences or patterns were found. At all times there were areas with egg numbers below those considered economically serious; this finding has been utilized in new control strategy and tactics that have been effectively implemented both experimentally and commercially. Spraying against larvae appeared also to reduce oviposition for at least 3 days, but could account for only some of the differences between areas. These findings suggest redistribution of mobile populations of moths over large dis• tances, and the dominant, contemporary, synoptic, and mesoscale weather patterns were considered as possible agencies operating on appropriate scales. The most vigorous systems are the outflows from rainstorms, and a s t a t i s t i c a l l y s i g n i f i c a n t relationship was found between the distribution of rain and of H. armigera eggs. In each of the seven seasons 1970- 1976, in the 3 days immediately following rainfall that was widespread in the Gezira, H. armigera laying at increased density reaching economically significant levels was reported, but over the areas outside and adjoining the rain, and not within the rain area itself. In addi• tion, the seasonal southward movement of the intertropical discontinuity across northern Sudan tends to occur in an irregular series of to-and-fro surges of 400 km' or more in a period of 2 to 5 days; in three seasons, the peak laying coincided with one of these southward surges and may have been associated with it, but in a manner not yet understood. These two associations are suggested as being of value for forecasting localized areas potentially at greatest immediate risk of heavy attack by H. armigera.

*Centre for Overseas Pest Research, London, UK.

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management 15-20 November 1981, Patancheru, A.P., India 8 7 continuellement, et I'on n'a pas trouve de difference ou systeme consistants. On a toujours t r o u v e des surfaces ayant un nombre d'oeuts sous des seuils c o n s i d e r e s comme e c o n o m i q u e - ment graves; cette decouverte a servi dans de nouvelles strategies et techniques de lutte qui ont ete utilisees de maniere efficace tant au niveau experimental que commercial. Une pulverisation contre les larves semblait aussi reduire I'oviposition pour au moins trois jours; mais ne comptait que pour quelques-unes des differences entre les zones. Ces observations semblent montrer une redistribution des populations mobiles de papil- lons sur de grandes distances et les regimes meteorologiques dominants, actuals synoptiques et a moyenne echelle seraient des agents eventuels operant sur des e c h e l l e s appropriees. L e s systemes les plus vigoureux sont les pluies violentes etil y a eu une relation statistique- ment significative entre la distribution des pluies et les oeufs d'H. a r m i g e r a . A chacune des sept saisons, 1970-1976, dans les trois jours suivant l es pluies qui couvraient largement la region de Gezira, H. armigera pondait a une densite accrue atteignant des niveaux econo- miquement significatifs, mais dans des aires non couvertes par la pluie ou attenantes aux aires pluvieuses, et non dans ces dernieres. De plus, le mouvement saisonnier vers le sud de la d i s c o n t i n u i t e intertropicale traversant le nord du Soudan tend a se manifester en series irregulieres de mouvements ponctuels de va-et-vient de 400 km2 ou plus dans une periode de 2 a 5 jours; au cours de trois saisons, le maximum de ponte a coincide avec I'un de ces mouvements puissants vers le sud et pourrait lui etre associe, mais de maniere encore non comprise. Ces deux associations pourraient servir a identifier les zones potentiellement le plus en danger immediat d'etre tortement attaquees par H. armigera.

In the Sudan Gezira Heliothis armigera (Hubner) present paper formed part of that project and were has been considered a major pest of cotton only undertaken to determine whether any large-scale since 1965 (Hassan 1970; Joyce 1976b). Its ovipo- patterns could be discerned in the distribution of H. sition is generally closely related to the flowering armigera eggs; in this, full use has been made of the period of its host plants (Pearson 1958), but in the intensive survey data and other findings of the pro- Gezira, although the irrigated cotton remains ject. Egg counts were used as evidence of recent apparently suitable as a host plant for H. armigera activity by the female moths, since the eggs hatch until December, eggs are laid on Gossypium bar- in 2 days in the Gezira (Balla 1970), and because badense in numbers of economic importance only the numbers of H. armigera attracted to light-traps from early September to early November; i.e., from proved to be very small, limiting the value of this a few weeks after sowing and before the formation approach (Bowden and Gibbs 1973). of fruiting buds, until after flowering has started in It was first noted in 1970 that throughout the mid-October and the first bolls are forming (Joyce Gezira as a whole, the distribution of H. armigera 1976b). Local practice was to use persistent insec• eggs appeared to be "clumpy rather than random; ticides in the 1970s—about four applications i.e., that when there were high counts in one 'Block', directed against bollworm larvae and two later often there were eggs in numbers in adjacent sprays against other pests, particularly whitefly. 'Blocks' at about the same time" (Haggis 1970).1 In 1970 a multidisciplinary research project was This inference was tested statistically, using data begun in the Gezira, at the request of the Sudan from later seasons, as described in the first part of Ministry of Agriculture, to develop and improve this paper (and see Haggis 1981). Variations in the crop-protection methods. Initially, emphasis was spatial and temporal distribution of H. armigera laid on detecting the adult stages of insect pests, in may be related to a number of causes, both biologi• particular H. armigera, to discover their distribution cal and physical; better knowledge of them might and potential as spray targets (Joyce 1976b). At the enable areas under immediate threat to be identi• end of 2 years' large-scale field trials it was con• fied more speedily. The cessation of important egg- cluded that timely application of nonpersistent insecticides, applied when H. armigera laying was approaching its peak so that the chemical contami• 1 nated the plants at the time of maximum hatching, M.J. Haggis, 1970, Relationship between American bollworm in the Gezira and the lnter-Tropical Front. Report to the Plant Protec- was effective (Russell-Smith, in Haggis 1973). tion Division, Sudan Ministry of Agriculture, November 1970, The biogeographical studies described in the (unpublished typescript).

8 8 laying by H. armigera usually closely coincides with 2 8 0 m (90 f e d d a n s or 37.8 ha). the e n d of t h e m o n s o o n s e a s o n a n d the departure southwards of the intertropical convergence zone, a n d winds w e r e already k n o w n to c o n c e n t r a t e or Distribution of Heliothis armigera disperse insects of many species (e.g. Rainey 1963, 1976; Johnson 1969); therefore, one aspect Eggs of the present studies, d e s c r i b e d in the s e c o n d part of this paper, was directed to assessing whether Data and Methods the distribution of ovipositing moths was more closely related to the major windfields and whether T h e S G B survey data on H. armigera egg c o u n t s for these c o u l d be used for forecasting, as for the e a c h season, 1 9 7 0 to 1976, a n d all parts of the desert locust and African armyworm (Betts 1976). irrigated area w e r e extracted from the files of the Other associated contemporary studies in the pro• Chief Entomologist, and the mean numbers of eggs ject investigated the distribution of airborne insects per block were plotted, for most years on daily map in relation to winds (Bowden and Gibbs 1973; Rai• series. At this time, insect survey counts were usu• ney 1976; Schaefer 1976), and the importance of ally expressed as numbers per 3-m row; this was other host plants (Joyce 1976b; Topper 1978). adopted as the basic unit for these analyses, and as spraying was recommended at two or more H. armigera eggs or larvae per 3-m (Balla, in Haggis, Description of the Site 1973), this has been used as a convenient refer• e n c e level. At the standard spacing of 50 x 80 cm The Sudan Gezira is uniquely homogeneous in its a n d three cotton plants per station, the 3 - m row 2 topography, climate, farming methods, crops, and represents 18 plants and a sample of 2.4 m . Within pest survey and control practices. It occupies a each block, usually six such samples were taken in roughly triangular area of some 25 000 km2 each of six to ten fields at 3- to 6-day intervals. T h e b e t w e e n the Blue a n d White Niles and is a feature• detailed counts made in individual fields including, less clay plain over m u c h of w h i c h the gradients since 1973, the intensive survey counts made are too gentle to be visibly perceptible. T h e irriga• every 3 days to meet the requirements of the n e w tion system d e s c r i b e d in detail by Allan a n d Smith spray program of the project (Joyce 1975; Russell- (1948), now covers 8400 km2 . Cotton is the most Smith 1975), m a d e possible m o r e detailed study by important c a s h crop, with s o m e 2 0 0 000 ha planted using m a p s of a s c a l e large e n o u g h to permit pre• annually. The agronomy and farming practices are cise location of each field. These counts were sim• closely controlled by the S u d a n Gezira B o a r d ilarly plotted on daily maps. Both map series were (SGB); for example, sowing is scheduled to take designed to s h o w rises a n d falls as well as actual place within a period of 2 w e e k s over the entire levels of infestation. Gezira, around the end of July. Up to 1975 the To e x a m i n e the c h a n g i n g distribution of H. cotton g r o w n w a s mainly G. barbadense, variety armigera eggs through t h e season, the e g g c o u n t s Barakat, with also some earlier flowering G. hirsu- of 1971 and 1975 (transformed to logarithms) were tum, variety Acala, chiefly in the north; both strains subjected to analyses of variance, using 3-day are highly resistant to blackarm disease, which at periods (omitting Fridays), as described elsewhere one time was a major problem there. A number of (Haggis 1981). A grid was superimposed on the other agronomic changes also have been intro• detailed m a p s to give respectively units of 6 0 0 to d u c e d in recent years: e.g. during the late 1960s to 700 km2 a n d 8 0 0 to 9 0 0 km2 , in e a c h of w h i c h s o m e early 1970s, the area of lubia ( D o l i c h o s lablab L.) 5 to 50 fields were sampled in e a c h 3-day period; sown in September, was progressively replaced for both years the m a p s of block m e a n e g g c o u n t s with groundnut (Arachis hypogaea L.), w h i c h is w e r e divided into s e v e n areas 1000 to 2 0 0 0 k m2 in s o w n in July a n d begins flowering in late August, extent. and further changes in the rotation greatly reduced the annual a c r e a g e of fallow after the mid-1970s. Results For administrative and operational purposes, the Gezira is subdivided into m o r e than 100 units called T h e m e a n n u m b e r s of H. armigera e g g s in 1971 in Blocks, w h i c h vary in size a n d c o m p r i s e b e t w e e n each of the eight small grid sections (600-700 km2 ) 50 and 400 fields. The size of most fields is 1350 x are presented in Figure 1, w h i c h s h o w s that there

8 9 Figure 1. Mean numbers of H. a r m i g e r a eggs per 3-m row from 21 September to 1 November 1971, in small sections, showing the largest and smallest standard errors. The map shows the boundaries of the sections over the area (shaded) for which detailed counts were available.

9 0 were conspicuous differences between sections of the project, and differences at the 1.0% level only and with time, during the season. The highest and in NC, into which the project extended. Analyses of most widespread peak in period 10 (23-25 the detailed egg counts of the project area (divided October) included means of 11.2 eggs per 3 m in into five sections of 800-900 km2 ) for t h e first half of Section 8 and 7.6 in Section 7, which together the season showed that they varied very signifi• represented the highest egg counts of the season cantly more (at the 0.1% or 1.0% levels) between anywhere in the Gezira, although four sections sections than within them in four of the six periods, showed little or no increase in numbers at this time. and with time in all five sections. In five of the six In sections 2, 4, and 6, the density was usually less periods, two to four sections had mean egg than two eggs per 3-m row, while in Section 1 it was numbers below the level considered as threatening rarely below this level. economic loss. The analyses of these detailed egg counts Thus these analyses confirmed the findings from showed that differences between sections were 1971, that over large areas from several hundred to highly significantly greater (at the 0.1% level) than some thousands of square kilometers, the levels of within them in all periods except the first (5%) and H. armigera oviposition on cotton usually varied ninth (not significant), and that for each section significantly less within areas than between them; differences were highly significantly greater (at the that there were no consistent differences or pat• 0.1% or 1.0% levels) between periods than within terns; that at any time substantial areas had egg t h e m . numbers below those considered economically The changing levels of egg numbers in the larger serious; and that the boundaries of such areas area units for the same period and part of the changed continually. Gezira are shown in Figure 2; the individual areas In a study based on intensive counts over two are named geographically—North, North-Central, blocks, it was found that egg numbers were etc. Despite marked differences between north and reduced in the period immediately following spray• south, each area showed at times similarities to the ing (Russell-Smith 1975; Joyce 1976b). Although area(s) adjacent to it. However, between no two the earlier control measures had been directed periods was the trend the same in all areas. Tests against larvae, the present studies found a similar using least significant differences showed that in all effect in the SGB block mean egg counts of 1971 : periods except 4 and 6, there were significant dif• of 64 cases in that season where blocks were ferences between two or more of the seven areas, known to have been counted within 3 days both and in all but one period, between areas that were before and after the date of spraying, only three adjacent or adjoining. cases showed any increase in egg numbers imme• Comparison of the curves for the NC, SEC, and diately after spraying; in 16 cases decreases were SE Areas and those of their constituent sections by a factor of 10 or m o r e , including 5 by a factor of > showed that similarities between them varied with 20. Two of the increases were fourfold to > 5.0 eggs time, and changes in level of infestation in an area per 3 m; o n e of these, in NC A r e a , o c c u r r e d d u r i n g could be dominated by the number of eggs in one the mid-October peak; the other, in SE, was during part, rather than in the whole of it, but that within the massive peak there later in the month (Fig. 2), individual areas of 1000 to 2000 km2 , no one sec• suggesting that in these cases the numbers of tion (600-700 km2 ) predominated throughout the moths available to invade the cotton from localities s e a s o n . not currently under spraying far exceeded the Similar analyses of the 1975 block mean egg numbers that may have been killed. counts in the same seven areas showed that in this When Sections 1 to 8 of the 1971 analysis were year egg numbers were generally highest in the N examined to see how far the significant differences Area, where the mean reached a record of 29 eggs between them might be attributable to effects of per 3-m row during 11 to 13 October; the main spraying, it w a s found that, while this might at least laying of the season was at this time in all areas in part account for some of the significant differen• except SEC, where there was a minor peak. Differ• ces between sections, less than half of them could ences between areas were highly significant, at the be attributed to this cause. Indeed, some of the 0.1 % or 1.0% levels, in 8 of the 12 periods; however, differences might have been even more marked in between periods, differences at the 0.1% level were the absence of spraying. found only in SEC and SE Areas, which were almost A fuller description of these analyses can be entirely covered by the intensive sampling system found elsewhere (Haggis 1981).

91 1971 Sept. O c t o b e r N o v . Sept. O c t o b e r N o v . 21 1 10 2 0 1 21 1 10 20 1 Period 12 3 4 5 6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12

4 N C : SEC N:NC

3 NC

2 NC

SEC 0 . 5

SEC:SE 8 0 25 7 km 6

5 N 15°N 4

3 SE NC 2

WC 1 SEC

SEC SE 0 . 5 SWC

Period 1 2 3 4 5 6 7 8 9 10 11 12 21 1 10 2 0 1 33°E 1971 Sept. O c t o b e r N o v .

Figure 2. Mean number of H. armigera eggs per 3-m row from 21 September to 1 November 1971 over large areas of the Old Gezira, showing similarities and differences between adjoining areas. Largest and smallest standard errors for each area shown on relevant graphs and key to areas and symbols on the map.

9 2 Discussion found to be an important breeding area and source of H. armigera populations and also to provide local These analyses are believed to have been the first roosting sites by day for moths laying on the neigh • to consider statistically the distribution of H. armig• boring cotton by night. The increase in levels of H. era egg-laying over the 8400 km2 area of the Gezira armigera infestation requiring corresponding as a whole. In 1971 it was found (Joyce 1976b) that increases in control measures since the introduc• over an experimental area of two adjacent blocks tion of groundnut into the Gezira rotation have bee n (200 km2 ) containing 4000 ha of cotton, the recognized (El Tigani and El Tagib 1978); the role of numbers of eggs rose and fell synchronously. The groundnut in changes in H. armigera distribution of present analyses extend this finding to show that the scale and type reported in the present paper over periods of 3 days there was significantly more merits further study in the light of the relevant agro• variability in oviposition between than within areas nomic data. 2 of 600 to 700 km (i.e., about six times the area of The fact that there can be a simultaneous and individual blocks), and that frequently such areas of sudden onset of widespread and heavy oviposition simultaneous rise or fall were of some thousands of despite extensive spraying within the same square kilometers, but that their boundaries areas—as in SE Area in late October 1971, when changed continually. Within each period, areas of there was almost a tenfold increase in egg 2 1300 km or greater (two or more sections) had egg numbers over 1200 km2 (Fig. 2)—suggests that numbers below the level considered economically those eggs must have been deposited by newly threatening. The implications of this finding for c o n • arrived moths from an unsprayed area, for locally trol strategy and tactics have already been dis• emerging ones would have been subjected to cussed (Joyce 1975, 1976a). Its particular insecticide, often before they had time to lay eggs significance has been to demonstrate that spray at 3 to 4 days old (Balla 1970). Such oviposition aircraft serving in areas with negligible infestation peaks, and similar widespread simultaneous sud• may safely be redeployed temporarily to reinforce den rises in H. armigera egg numbers in the new operations elsewhere. Since 1973 these tactics, Rahad Scheme to the southeast of the Gezira, together with the effect of the insecticide on adult recorded in 2 years before groundnut was intro• moths, have been utilized in the commercial pro• duced into the cropping there (R.J.V. Joyce, per• gram carried out alongside the research project; sonal communication), appear likely to be due to the consequent improvement in control has con• mass immigration by moths, possibly over at least sistently been reflected in the high cotton yields tens of kilometers. The highly significant changes within the project area (Joyce 1978,1980). in distribution, e.g., between Periods 1 and 2 (21 -27

On the scales of these analyses and apart from Sept) in Sections 4 and 6, and between Periods 7 spray effects, no consistent differences or patterns and 8(12-18 Oct) in Sections 1 and3 (Fig. 1), when of change were found in the distribution of H. armig- in both cases the Gezira mean egg numbers era eggs. This would conform with the degree of remained constant or comparable (see Fig. 5), also uniformity in the terrain and in the cropping of th e strongly suggest redistribution of ovipositing moths irrigated area. Therefore other agents that might over similar distances. In other insects mass immi• influence the distribution of oviposition were cons i • gration is associated with particular meteorological dered. Earlier studies had found relationships conditions operating on comparable scales (Rai- between the incidence of other pests and rainfall ney 1963, 1976; Johnson 1969). (e.g. Joyce 1961), but this approach initially proved inconclusive for H. armigera as counted on irri• gated cotton, though some such relationship due to Distribution of H. armigera Eggs host-plant availability might be expected in the in Relation to Weather adjacent grasslands across the Blue Nile, where vast numbers of larvae were observed (R.J.V. The main weather feature of the Gezira area during Joyce and N. Russell-Smith, personal communica• September to early November is the retreating tion). While no association with other host plants intertropical convergence zone (ITCZ) as the could be determined in the early years (Russell- southerly monsoon gradually gives way to the Smith, in Joyce 1976b), in more recent studies northerly trade winds, with the storm cells made in a single block under the new, more inten• embedded in the ITCZ system intermittently and sive crop rotation (Topper 1978), groundnut was briefly superimposing much stronger, but relatively

9 3 local, windfields on the area. Observations with 1969). The outflows associated with such meso- modified marine radar in the southern Gezira scale rainstorms have been identified as the showed that within storm outflow fronts insects strongest windfields in the Gezira area (Bhalotra could be 60 times more dense than in the air ahead 1958, 1959). of the front; they appeared on the radar display as a line-echo or arc, up to 20 km ahead of the precipita• tion and initially accelerating away from it, and Data and Methods coming to a halt only when the storm had decayed (Schaefer 1976). Radar, ground observations, and This study was limited to indirect observations on light-trapping showed that these lines consisted of the effects of windfields on the distribution of ovi• insects of many species, including moths. Line- positing H. armigera moths by the absence of a echoes from insects, albeit less well marked than close network of weather stations and of immediate those at storm outflows, were observed by the knowledge of the moth's behavioral and physiolog• radar in the ITCZ also, at the main wind shift ical responses to physical stimuli, such as changes (Schaefer 1976), and the highest numbers of in humidity. Temperature changes were consi• insects of several species were caught in suction dered probably too small to be a major influence on traps in the hours when this system passed over• moth behavior, since the mean daily range is of head (Bowden and Gibbs 1973; Russell-Smith in only 11 to 14°C in this season and at this latitude Joyce 1976b). (Ireland 1948). In addition to the insect survey data already de• scribed, the distribution of rainfall is recorded in an Description of the Weather exceptionally dense network of raingauges oper• ated by the SGB throughout the Gezira, with some 2 The synoptic-scale weather system dominating 300 gauges within a general area of 10 000 km . the area during September to early November is These could provide circumstantial evidence on the intertropical convergence zone (ITCZ), which possible winds associated with storms, if the rain during the northern summer lies a few hundred areas are regarded, on the radar evidence, as cen• kilometers north of Khartoum, separating dry, ters from which squalls, carrying lines of insects, warmer, northern-hemisphere air from moist, could have been moving out. Attention was con• cooler air of southern-hemisphere origin (Osman centrated on occasions when rain was widespread and Hastonrath 1969). The boundary between the in the Gezira, defined for present purposes as two, now called the intertropical discontinuity (ITD) recorded in at least 18 adjacent blocks, i.e., over 2 is frequently very marked at low level (e.g. Rainey some 1500 km . For each case study the rainfall 1976; Balogun 1981). Its position can be readily distribution was mapped in detail. To assess the inferred from the surface wind directions and dew immediate possible effect of a storm on moth distri• points of the regular synoptic observations and is bution, only those egg counts were used that were routinely plotted on the surface analyses of the made during the 3 days following the rainfall con• Khartoum Meteorological Department. The south• cerned. Although the eggs of some insects may be ward shift of the ITD, following the sun, begins washed off plants by rain, this effect has not been about mid-September and proceeds in irregular observed for H. armigera in the Gezira (I. Outram, stages with relatively small diurnal fluctuations personal communication). superimposed. The position of the ITD across eastern Sudan, as The rains that accompany its seasonal move• plotted on the routine 3-hourly synoptic charts, wa s ments occur from May to October, with amounts made available by the Khartoum Meteorological decreasing from a mean annual total of 400 mm at Department (from 1971 to 1976 transmitted for cur• Wad Medani in the southeast to 160 mm at Khar• rent use by the project), and plotted on daily maps . toum in the north (Ireland 1948). Local incidence of As the usual orientation of the ITD over this part of storms is very irregular: they are more frequent in Sudan is approximately northeast-southwest, its the central and southern Gezira, as convective movements were measured relative to a line pass• clouds, with associated low-level wind conver• ing through Khartoum and Wad Medani, roughly gence, develop where the underlying moist air is northwest-southeast, and conveniently represent• sufficiently deep, usually some 300 km to the south ing the long axis of the Gezira. For each of these of the position of the ITD at the surface (Pedgley seasons and 1970 this movement of the ITD was

94 presented graphically, relative to the Khartoum- Wad Medani line; the mean daily numbers of H. armigera eggs throughout the Gezira, computed from the block means, were plotted against the same time axes.

Results

Plots of the daily extent of rainfall and the daily numbers of blocks recording economically serious infestations of H. armigera eggs showed that the numbers of blocks with many eggs frequently increased immediately after rain in the Gezira. The daily maps of these data showed that, in each year, in the 3 days after widespread rain (as defined), egg numbers were indeed found extensively at increased density, but that the highest counts were generally outside or on the edge of the rain, with only small numbers of eggs recorded within the rain area itself. For example, on 17 Sept 1973, rain fell in 30 contiguous blocks of the Old Gezira and in 12 blocks of the Managil Extension (Fig. 3). Insect surveys were already in progress in most areas. Figure 3. Distribution of rainfall on 17 S e p - During 18 to 20 September, H. armigera egg tember 1973 and mean numbers of H. armigera numbers increased in many blocks, in 10 blocks to eggs in blocks counted from 18 to 20 more than double the numbers counted during the September. previous 3 days. All the high counts were outside the main rain areas; the daily maps showed that within the rain areas, in four blocks egg numbers edge of the rain areas increased sharply to exceed fell to half their earlier value, and three blocks that those outside (Fig. 4). Visual inspection of the less recorded markedly increased numbers neverthe• complete plots for a further four occasions sug• less had mean egg counts below the reference gested a similar egg distribution pattern for three of level of two eggs per 3 m. In the central Managil, t h e m . some egg numbers may have been suppressed by An example of the irregularity of the displace• spraying, which was completed immediately ments of the ITD is provided in Figure 5, in which before the counts were made. In many of the blocks the upper line represents the movements of the ITD unshaded on Figure 3, no counts were made relative to the Khartoum-Wad Medani line, and the because spraying was in progress 16 to 19 map has been skewed accordingly. The lower October. curve represents the daily mean numbers of H. There were altogether 17 occasions over the armigera eggs throughout the Gezira, and attention seven seasons 1970 to 1976 when rain was wide• is drawn to the very close agreement repeatedly spread (as defined) and the insect counts were shown between the mean numbers on successive adequate for statistical treatment. Analyses of var• days, for which the figures relate to sampling in iance showed a significant (5%) interaction completely different sets of blocks. between the numbers of eggs inside and those on The coincidence over 4 to 5 days of increased H. the edge of and outside the rain areas immediately armigera laying (the season's peak) and a strong before and after the rain: while egg numbers southward surge of the ITD from far north of the increased outside and on the edge of the rain, over Gezira beyond Atbara to south of Sennar (400-500 the next 3 days oviposition within the rain area km) was first noted in 1970. There were similar continued at the same level as before the storm. coincidences in each of the four subsequent sea• However, this effect did not persist, and in the fol• sons, although in three cases they occurred near lowing 3-day period egg numbers within and on the the start of the season, when an increase in egg

9 5 w a r d s into or across the Gezira. T h e e x c e p t i o n w a s 3.0 SE A r e a in Period 11 ( 2 6 - 2 8 Oct): t h e ITD h a d t r a v e r s e d t h e Gezira immediately prior to this period, w h e n it r e m a i n e d to t h e south b e y o n d S e n - nar, a n d e g g n u m b e r s , w h i c h w e r e generally d e • clining, remained high in the southeast (Figs. 2 and 5).

2 . 0 Discussion

Eggs counted Direct evidence of the influence of windfields on i n s i d e r a i n a r e a s flying insects in the Gezira has c o m e f r o m trapping o n e d g e o f r a i n and radar studies (Bowden and Gibbs 1973; Rai- 1.0- o u t s i d e r a i n a r e a s ney 1976; Schaefer 1976). The present studies of more indirect, circumstantial evidence have like• wise f o u n d significant association b e t w e e n the dis• 1-3 d a y s 1-3 d a y s 4-6 d a y s b e f o r e r a i n a f t e r r a i n a f t e r r a i n tribution of ovipositing H. armigera moths a n d the contemporary weather. The rainstorms considered Dates of counting here certainly will have caused brief disturbances in the windfield—mainly in the first half of the night, Figure 4. Numbers of H. armigera eggs before w h e n the m o t h s are most a c t i v e — a n d t h e radar and after widespread rainfall in the Gezira: observations have s u g g e s t e d a plausible m e c h a • means of 17 occasions, 1970-1976. nism that could at least in part explain the signifi• cant spatial pattern found, e v e n t h o u g h the exact cause of egg laying temporarily increasing only numbers could have been expected. However in outside and on the edge of areas of rainfall is not yet 1971 a n d 1 9 7 3 t h e heaviest laying of the s e a s o n understood. Whatever the causes, the finding again c o i n c i d e d with t h e most extensive s o u t h w a r d c o u l d still be of value for forecasting localized movement of the ITD. In 1971 this was near the end areas of potential major attack, such as in Figure 3, of the s e a s o n : while t h e ITD m o v e d 6 0 0 km f r o m if i m m e d i a t e k n o w l e d g e w e r e available of t h e daily a r o u n d A t b a r a a t 0 0 0 0 G M T o n 2 2 O c t o b e r t o south rainfall distribution, e.g., as observed by weather of Roseires by 0 6 0 0 G M T on 25 O c t o b e r (Fig. 5), radar. This would enable the main survey effort to altogether 40 blocks reported economically signifi- be c o n c e n t r a t e d outside the rain areas a n d in the cant numbers of eggs; four blocks with means of > areas where laying is likely to be heaviest, thereby 10 per 3 m a n d nine with m e a n s of > 5 e g g s per 3 m identifying more quickly the zones of serious egg w e r e c o u n t e d in 2 days, a n d t h e heavy oviposition infestation most immediately requiring control. w a s c o n c e n t r a t e d in t h e southeastern Gezira. T h e significance of this peak and the distribution of the The apparent association between H. armigera eggs has already been discussed (Fig. 2 and Hag• laying and movements of the ITD is difficult to gis 1981). assess, for there is no obvious mechanism for con• It w a s also n o t e d in 1 9 7 0 that w h e n blocks centrating insects ahead of the system when it is reported high n u m b e r s of H. armigera e g g s - moving southwards. It may still be valid to antici• a b o v e 5 per 3 - m r o w — m o s t often t h e I T D w a s pate a general i n c r e a s e in oviposition at s u c h a c l o s e over t h e s e b l o c k s , a n d that high m e a n e g g time; indeed, one was tentatively forecast by the c o u n t s also o c c u r r e d w h e n t h e I T D lay t o t h e north author a n d t h e late N. Russell-Smith on 6 O c t 1973, of the blocks concerned, but not when it was to the at t h e beginning of t h e m a i n ITD m o v e m e n t a n d south. In 1971 (using t h e 1 0 0 0 to 2 0 0 0 k m2 a r e a s of before t h e initial rise in e g g n u m b e r s , heralding t h e the earlier analyses), out of 80 area/periods, there peak laying of that season, was reported. A similar w e r e 1 7 w h e n t h e a r e a m e a n e g g c o u n t e x c e e d e d forecast in early October 1976 was less success• t w o per 3 - m row. For nine of t h e s e , on o n e or m o r e ful, for although t h e ITD m o v e d south 8 0 0 km f r o m of the nights w h e n t h e e g g s w o u l d h a v e b e e n laid, W a d i Haifa into t h e Gezira, H. armigera e g g t h e ITD h a d b e e n over t h e a r e a a t 1 8 0 0 G M T , a n d numbers remained very low, both through that for seven others, the ITD was moving rapidly south- period a n d for t h e rest of t h e s e a s o n .

96 Figure 5. Six-hourly positions of the inter-tropical discontinuity (ITD) relative to the Khartoum-Wad Medani line, and mean numbers of H. a r m i g e r a eggs counted daily throughout the Gezira, 7 Sept-7 Nov 1971. Extent of Gezira scheme shaded on upper graph. General Conclusions BHALOTRA, Y.P.R. 1958. Dust storms at Khartoum. Sudan Meteorological Service Memoir 1, Sudan Survey Department, Khartoum, Sudan. 74 pp. The distribution of H. armigera oviposition in the Sudan Gezira has been found to vary significantly BHALOTRA, Y.P.R. 1959. Adverse weather conditions less within than between areas that extended over at Khartoum, El Obeid and Wadi Haifa. Sudan Meteoro• hundreds to thousands of square kilometers, but logical Service Memoir 2, Sudan Survey Department, whose boundaries changed continually. At all Khartoum, Sudan. 112 pp. times there were areas where egg numbers were BOWDEN, J., and GIBBS, D.G. 1973. Light-trap and below the economic threshold. These findings suction-trap catches of insects in the northern Gezira, have proved of value for control strategy and tac• Sudan in the season of southward movement of the Inter- tics. The spatial and temporal associations found Tropical Front. Bulletin of Entomological Research 62: b e t w e e n H. armigera oviposition and rainfall and 571 -596. perhaps also the ITD are considered sufficiently EL TIGANI, M., and EL TAGIB, M. 1978. Development strong to be of immediate value for forecasting of crop protection in the Sudan, with special reference to where and when potentially serious attacks may application of ULV and water-based insecticides. Pages occur, even though the mechanisms for these 149-163 in Proceedings, Fourth Scientific Conference on associations are not yet understood and require Chemicalisation of Plant Production in the Tropics and further research. Subtropics, Volume 3. Institut fur tropische Landwirt- schaft, Karl-Marx Universitat, Leipzig, German Demo• cratic Republic.

Acknowledgments HAGGIS, M.J. 1973. Insect flight and its relevance to the strategy of control of insect pests of cotton in the Thanks are particularly due to Professor R.J.V. Sudan Gezira. Pest Articles and News Summary 19:419- Joyce, the Research Director of the project in the 421. early 1970s, and to his successor and other HAGGIS, M.J. 1981. Spatial and temporal changes in members of the team, for their help and stimulating the distribution of eggs of Heliothis armiger (Hubner) discussions over the years, and to Miss S.M.Green, (Lepidoptera: Noctuidae) on cotton in the Sudan Gezira. Statistician at COPR, for invaluable guidance on Bulletin of Entomological Research. 71: 181-193. the treatment and presentation of the data. The data and other facilities provided by the Sudan HASSAN, H.M. 1970. Progress in chemical control of pests of cotton in the Gezira. Pages 232-246 in Cotton Gezira Board, by the Sudan Meteorological Depart• growth in the Gezira environment: A symposium to mark ment, and by CIBA-GEIGY, who also sponsored the 50th anniversary of the Gezira Research Station (eds. the fieldwork, are gratefully acknowledged. MA. Siddiq and L.C. Hughes), Wad Medani, Sudan: Agri• cultural Research Corporation. 318 pp.

IRELAND, A.W. 1948. The climate of the Sudan. Pages References 62-83 in Agriculture in the Sudan, ed. J.D. Tothill. London, UK: Oxford University Press. 974 pp.

ALLAN, W.N., and SMITH, R.J. 1948. Irrigation in the JOHNSON, C.G. 1969. Migration and dispersal of Sudan. Pages 593-632 in Agriculture in the Sudan, ed. insects by flight. London, UK: Methuen. 763 pp. J.D. Tothill. London, UK: Oxford University Press. 974 pp. JOYCE, R.J.V. 1961. Some factors affecting numbers of BALLA, A.N. 1970. American bollworm in the Gezira Empoasca lybica (De Berg.) (Homoptera: Cicadellidae) and Managil. Pages 281-292 in Cotton growth in the infesting cotton in the Sudan Gezira. Bulletin of Entomo• Gezira environment: a symposium to mark the 50th anni• logical Research 52: 191 -232. versary of the Gezira Research Station, eds. M.A. Siddiq JOYCE, R.J.V. 1975. The implications to control stra• and L.C. Hughes. Wad Medani, Sudan: Agricultural tegy of the observed flight activity of pest species in the Research Corporation. 318 pp. Sudan Gezira. In Proceedings, Seminar on the Strategy BALOGUN, E.E. 1981. Seasonal and spatial variations for Cotton Pest Control in the Sudan Gezira. CIBA-GEIGY, in thunderstorm activity over Nigeria. Weather (London) Wad Medani, Sudan. 36: 192-197. JOYCE, R.J.V. 1976a. Sequential aerial spraying of cot• BETTS, E. 1976. Forecasting infestations of tropical ton at ULV rates in the Sudan Gezira as a contribution to migrant pests: desert locust and the African armyworm. synchronised chemical application over the area occu• Pages 113-118/ in Insect flight, ed. R.C. Rainey. Symposia pied by the pest population. Pages 47-54 in Proceedings, of the Royal Entomological Society of London 7, Oxford, Fifth International Agricultural Aviation Congress. Inter• UK: Blackwell. national Agricultural Aviation Centre, UK. 403 pp.

9 8 JOYCE, R.J.V. 1976b. Insect flight in relation to problems of pest control. Pages 135-155 in Insect flight (ed. R.C. Rainey). Symposia of the Royal Entomological Society of London 7. Oxford, UK: Blackwell.

JOYCE, R.J.V. 1978. Yield response of Gossypium barbadense in the Sudan Gezira to aerial spraying at ULV rates with Nuvacron 40® Pages 229-242 in Pro- ceedings, Third Seminar on the Strategy for Cotton Pest Control in the Sudan. CIBA-GEIGY, Basel, Switzerland. 357 pp.

JOYCE, R.J.V. 1980. Aircraft equipment and biological objectives. Pages 13-22 in Trends in airborne equipment for agriculture and other areas. Aero-Agro 1978. Pro- ceedings of a Seminar Organized by the United Nations Economic Commission for Europe. 18-22 Sept 1978, Warsaw, Poland. Oxford, UK: Pergamon Press. 358 pp.

OSMAN, O.E.,and HASTENRATH, S.L. 1969. On the synoptic climatology of summer rainfall over central Sudan. Archiv fur Meteorologie, Geophysik und Bioklima- tologie, Serie B 17: 297-324.

PEARSON, E.O. 1958. The insect pests of cotton in tropical Africa. London, UK: Empire Cotton Growing Corp. and Commonwealth Institute of Entomology. 355 pp.

PEDGLEY, D.E. 1969. Diurnal variation of the incidence of monsoon rainfall over the Sudan: Part I and II. Meteoro- logical Magazine (London) 98: 97-107,129-134.

RAINEY, R.C. 1963. Meteorology and migration of desert locusts: applications of synoptic meteorology in locust control. World Meteorological Organization Tech- nical Notes 54. Geneva, Switzerland: WMO.

RAINEY, R.C. 1976. Flight behavior and features of the atmospheric environment. Pages 75-112 in Insect flight (ed. R.C. Rainey). Symposia of the Royal Entomological Society of London 7. Oxford, UK: Blackwell. 287 pp.

RUSSELL-SMITH, N.A. 1975. The distribution and sampling of Heliothis armigera (Hb.) eggs on cotton in the Sudan Gezira. In Proceedings, Seminar on the Strategy for Cotton Pest Control in the Sudan Gezira. CIBA-GEIGY, Wad Medani, Sudan.

SCHAEFER, G.W. 1976. Radar observations of insect flight. Pages 157-197 in Insect flight (ed. R.C. Rainey). Symposia of the Royal Entomological Society of London 7. Oxford. UK: Blackwell. 287 pp.

TOPPER, C. 1978. The incidence of Heliothis armigera larvae and adults on groundnuts and sorghum and the prediction of oviposition on cotton. Pages 17-33 in Pro- ceedings, Third Seminar on the Strategy for Cotton Pest Control in the Sudan. CIBA-GEIGY, Basel, Switzerland.

99 Discussion — Session 2

Dr. Hartstack confirmed that there was good corre• migration from outside the area. Within the Gezira, lation between trap catches of moths and oviposi- Heliothis feeds on a range of crops, including cot• tion in crops in the area of more than 1000 ha of ton, groundnut, and sorghum. There is substantial land under his study in the USA. This had not yet movement of populations between these crops. been extended to an area that was anywhere near There appear to have been no other intensive stu• the size of the Sudan Gezira. Oviposition and the dies of oviposition by populations of Heliothis on an subsequent populations of larvae are known to be area as large as the Gezira anywhere else in the influenced by many factors, including rainfall, irri• world, but attempts are being made to monitor gation and other cultural practices, and parasites migrations of moths over large areas of USA. and predators. The individual effects of each ele• ment have yet to be quantified, but generalizations can be useful for modeling. It is not essential that all the factors affecting Heliothis populations be fully quantified before a model can become useful. When asked what proportion of Heliothis moths in any population migrate, Dr. Raulston could give no precise data; however, he said that Drs. Hughes and Fisher are currently studying the movement of Heliothis moths from the ground to different levels in the atmosphere. They are also recording the activity of moths in different crops by observation and trapping. The migration of moths to the south• ern USA is also being studied. Dr. Bartlett did not think that the disruption of long-range migrations of moths would reduce the vigor of a species by reducing genetic mixing. Most local populations already contain a great deal of genetic variation, as shown by electrophoretic analysis. Random mating within the population would maintain that heterozygosity in the Hardy - Weinberg equilibrium. Isozyme analysis is a conve• nient means of measuring genetic variability and should be used to distinguish geographic popula• tions in order to determine how important and extensive migration really is. There is no evidence that strains carrying genetic markers are electro- pnoretically distinguished from the wild strains of Heliothis. It is not clear whether rainfall directly stimulates oviposition by Heliothis or whether it does so indi• rectly, by stimulating crop growth, which then attracts oviposition. Dr. Haggis commented that there appear to be differential ovipositional responses to rainfall in irrigated and unirrigated fields. Work in the USA has shown an increased nectar flow in cotton after rainfall, which could influ• ence moth feeding and subsequent oviposition. But heavy rainfall could also wash the eggs off plants. The moth populations of the Sudan Gezira are not isolated, for they are known to be affected by

100 Session 3

Natural and Biological Control Elements

Chairman: B.R. Wiseman Rapporteurs: S. Sithanantham Cochairman: N.N. Ramakrishnan A.B. Mohammed

Prospects for Utilization of Parasites and Predators for Management of Heliothis Spp

E.G. King, J.E. Powell, and J.W. Smith*

Abstract

Naturally occurring predators and parasites (natural enemies) are important in regulating populations of Heliothis. Explicit instructions in insect control guides, developed through qualitative and quantitative evaluations ol natural enemies, are needed so that natural enemy numbers can be used more directly in decision-making. Many species ol natural enemies of Heliothis have been identified in every country where a search has been conducted. Fre• quently, Heliothis spp egg and larval parasitism levels are high, but a critical analysis must be conducted to assess the actual contribution of each species to Heliothis population reg• ulation. Opportunities exist tor importing and establishing exotic natural enemies in vacant niches (e.g., unattacked life stages, certain habitats or host plants), for displacing natural enemies that do not contribute to population regulation by more effective ones, and for estab• lishing natural enemies that have pesticide tolerance. Where natural enemy numbers are in• adequate for maintaining Heliothis populations at subeconomic levels, augmentation may be feasible. Performance of lower numbers of parasites may be improved by application of behav• ioral chemicals to mimic high host populations. Nevertheless, inexpensive rearing procedures, such as in vitro rearing, that result in a vigorous parasite or predator with essential behav• ioral characteristics intact over time, will have to be developed before augmentation by rear• ing and periodic release is economically feasible for most parasites and predators.

Heliothis spp feed on a wide range of wild and maintenance and increase of Heliothis p o p u l a • cultivated plants. Both wild and cultivated host tions; however, cultivated host crops (cotton, plants are important because they contribute to maize, soybeans, sorghum, groundnut, pigeonpea,

*U.S. Department of Agriculture, Agricultural Research Service, Bioenvironmental Insect Control Laboratory, Stoneville, Miss, USA.

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. 1 0 3 c h i c k p e a , t o b a c c o , a n d t o m a t o e s a n d other v e g e • H b n . with 134 species. T o d d (1978) also listed 14 tables) are of primary c o n c e r n , b e c a u s e of their Heliothis s p e c i e s for North A m e r i c a ( e x c l u d i n g e c o n o m i c value. In t h e U S A alone, a n n u a l losses of Hawaii), treating Helicoverpa as a s y n o n y m of Heli• over o n e billion dollars are attributed to Heliothis, othis; 13 s p e c i e s w e r e c o m m o n to H a r d w i c k ' s a n d n u m e r o u s other countries (e.g., India a n d A u s • (1970) list. Seventy-eight s p e c i e s a n d s u b s p e c i e s tralia) e x p e r i e n c e similar high losses ( s e e other of w o r l d Heliothis (excluding Schinia) were listed by p a p e r s in these Proceedings). T o d d (1978), for w h i c h he c r o s s - i n d e x e d 154 Heliothis larvae c o m p e t e with m a n for f o o d a n d s p e c i e s - g r o u p names. fiber, usually directly, by attacking t h e fruiting forms. Typically, the most severely d a m a g e d c r o p s are t h e cultivated annuals, w h i c h t e n d t o c o m p o s e Western Hemisphere a n unstable a g r o e c o s y s t e m . T o further c o m p o u n d t h e problem, high-yielding cultivars are often Heliothis zea a n d H. virescens are distributed s e l e c t e d without regard to Heliothis resistance, widely over North, Central, a n d South A m e r i c a , thus often requiring higher levels of pesticides, w h e r e they are e c o n o m i c a l l y important ( K o g a n et w h i c h are usually detrimental to natural e n e m y al. 1978). In t h e USA, t h e s e t w o s p e c i e s are most populations. a b u n d a n t in the southeast, with i m p o r t a n c e Nevertheless, naturally o c c u r r i n g predators a n d d e c r e a s i n g north a n d west of this region (Stinner et parasites are important in regulating n u m b e r s of al. 1980). T h e H. zea to H. virescens ratio fluctuates Heliothis ( Q u a i n t a n c e a n d Brues 1905; Fletcher greatly a c c o r d i n g to year, location, host crop, a n d a n d T h o m a s 1943; Ewing a n d Ivy 1943; W h i t c o m b c r o p phenology. Other North A m e r i c a n Heliothis a n d Bell 1964; V a n d e n B o s c h a n d H a g e n 1966; ( H a r d w i c k 1970; T o d d 1978) are less abundant a n d R i d g w a y et al. 1967; Lingren et al. 1968; Van den limited in distribution. Heliothis subflexa ( G u e n e e ) B o s c h et al. 1969). In the a b s e n c e of insecticides, is not e c o n o m i c a l l y important, a n d is k n o w n to f e e d t h e s e natural e n e m i e s often maintain Heliothis only on g r o u n d cherry, Physalis spp; it is well k n o w n populations at s u b e c o n o m i c levels in most crops. for its hybridization with H. virescens under labora• W h e r e this fails to h a p p e n b e c a u s e of i nad equ ate tory conditions (Laster 1972). T h e distribution of H. n u m b e r s of natural e n e m i e s , a u g m e n t a t i o n of subflexa ranges from Mississippi to T e x a s (Missis• beneficials m a y be feasible. Introduction a n d sippi: Smith et al. 1976a; Louisiana a n d A r k a n s a s : establishment of m o r e effective natural e n e m i e s Brazzel e t al. 1953; T e x a s : M l . Laster, Entomolo• also has potential. We s u m m a r i z e here the status of gist, Delta B r a n c h Experiment Station, Mississippi the u s e of predators a n d parasites for Heliothis Agricultural and Forestry Experiment Station, control, attempt to synthesize this information, a n d Stoneville, Mississippi, personal communication), s u g g e s t priority research for the future. M e x i c o ( M l . Laster, personal c o m m u n i c a t i o n ) , South A m e r i c a (Colombia: H a l l m a n 1980), a n d o n the island of St. Croix (M.L. Laster, personal Distribution and Abundance communication). of Heliothis Spp In South A m e r i c a , H. zea is distributed m o r e widely than H. virescens ( K o g a n et al. 1978). T h e T h e g e n u s Heliothis Ochsenheimer may contain gelotopoeon group (four species) is e n d e m i c to t h e most e c o n o m i c a l l y important g r o u p of insects South A m e r i c a . Heliothis gelotopoeon (Dyar) is in t h e w o r l d ( K o g a n et al. 1978). T h e c o r n e a r w o r m e c o n o m i c a l l y important in A r g e n t i n a ( H a r d w i c k c o m p l e x w a s e x a m i n e d b y H a r d w i c k (1965), w h o 1965) a n d coexists with H. atacamae (Hdwk.) in d e f i n e d t h e following five s p e c i e s groups within his central Chile. T h e latter s p e c i e s inhabits arid n e w g e n u s Helicoverpa: punctigera, gelotopoeon, regions of southern Peru a n d northern a n d central hawaiiensis, armigera, a n d zea. A l t h o u g h 17 s p e - Chile. c i e s w e r e p l a c e d in Helicoverpa Hdwk. ( H a r d w i c k 1965), all s p e c i e s are d i s c u s s e d herein under the g e n u s Heliothis. H a r d w i c k ' s (1970) g e n e r i c revi- Eastern Hemisphere sion of the North A m e r i c a n Heliothidinae, in w h i c h 158 s p e c i e s in 14 g e n e r a w e r e listed, i n c l u d e d o n e T h e most important agricultural pest in the e a s t e r n Helicoverpa a n d 13 Heliothis spp. This list w a s h e m i s p h e r e is H. armigera Hb. ( H a r d w i c k 1965). extensive b e c a u s e it i n c l u d e d the g e n u s Schinia This s p e c i e s o c c u r s widely in Europe, m u c h of

104 Africa, India, Asia, New Zealand, Australia, and on limited in distribution. In India, H. armigera has a several Pacific Islands. In Africa, H. armigera wide distribution and causes serious losses in o c c u r s with H. assulta G u e n e e , H. fletcheri (Hdwk.) many crops (Rao 1974), while H. assulta a n d H. a n d H. toddi (Hdwk.). Only the endemic H. helenae peltigera have limited host ranges and distribution. (Hdwk.) occurs on St. Helena Island, but H. assulta, In J a p a n , H. viriplaca adaucta Btlr. coexists with H. H. pacifica (Hdwk.), H. minuta (Hdwk.), H. confusa armigera where their geographic ranges overlap (Hdwk.), H. hawaiiensis Quaint. and Brues, and H. (Stinner et al. 1980). pallida (Hdwk.) occur on the Pacific Islands, in addition to H. armigera. In Australia, H. armigera is limited mainly to the Natural Enemies of Heliothis Spp coastal and subcoastal areas of eastern Australia and the North Territory (Common 1953). However, Parasites and predators that occur with Heliothis the indigenous H. punctigera Wallengren is widely spp in the USA and in other parts of the world are distributed, and occurs in every state. These two discussed below. species cause economic damage to many fruit, vegetable, and ornamental crops. Heliothis spp were reported in 1928 (Lea) to be a chief pest of Parasites in the USA lucerne in South Australia. Two Heliothis s p e c i e s that are not of pest status in Australia are assulta The value of natural control agents, particularly a n d rubrescens (Walker) (Common 1953). parasites in regulating pest species is becoming Heliothis spp are of considerable economic more apparent as research is conducted. The prin• importance on many Egyptian crops (Ibrahim cipal parasites that contribute to mortality of Helio- 1980). H. armigera is most abundant throughout this eggs and larvae are shown in Table 1. The Egypt, but peltigera (Denis and Schiff.) also occurs importance of egg and larval parasites of H. zea widely, while H. nubigera Herrick-Schaffer is more was recognized by Quaintance and Brues in 1905.

T a b l e 1 . P r i n c i p a l p a r a s i t e s o f H e l i o t h i s a p p .

P a r a s i t e R e f e r e n c e

USA

Hymenoptera: Braconidae Apanteles marginiventris ( C r e s s o n ) R i d g w a y a n d L i n g r e n 1 9 7 2 Cardiochiles nigriceps ( V i e r i c k ) S n o w e t a l . 1 9 6 6 : L e w i s a n d B r a z z e l 1 9 6 8 Microplitis croceipes ( C r e s s o n ) S n o w e t a l . 1 9 6 6 : L e w i s a n d B r a z z e l 1 9 6 8 Hymenoptera: Ichneumonidae Campoletis sonorensis ( C a m e r o n ) L i n g r e n e t a l . 1 9 7 0 Hymenoptera: Trichogrammatidae Trichogramma pretiosum R i l e y G r a h a m 1 9 7 0 : O a t m a n a n d P l a t n e r 1 9 7 1 T r i c h o g r a m m a exiguum P i n t o & P l a t n e r K i n g e t a l . , u n p u b l i s h e d d a t a D i p t e r a : T a c h i n i d a e Archytas marmoratus (Townsend) S h e p a r d a n d S t e r l i n g 1 9 7 2 Eucelatoria bryani S a b r o s k y B o t t r e l l e t a l . 1 9 6 8

A u s t r a l i a

Hymenoptera: Braconidae Microplitis demolitor W i l k i n s o n H a f e z 1 9 5 1 Hymenoptera: Ichneumonidae Heteropelma scaposum ( M o r l e y ) M . S h e p a r d , p e r s o n a l c o m m u n i c a t i o n

Continued

1 0 5 T a b l e 1. Continued

P a r a s i t e R e f e r e n c e

I n d i a

Hymenoptera: Braconidae Bracon brevicornis W e s m . Achan et al. 1968 Hymenoptera: Ichneumonidae Campoletis chlorideae U c h i d a R a o 1 9 7 4 Eriborus sp R a o 1 9 7 4 Hymenoptera: Trichogrammatidae Trichogramma s p p R a o 1 9 7 4 Diptera: Tachinidae Carcelia illota ( C u r r a n ) R a o 1 9 7 4 Goniophthalmus halli M e s n i l R a o 1 9 7 4 Palexorista laxa ( C u r r a n ) R a o 1 9 7 4

E u r o p e

Hymenoptera: Braconidae Apanteles kazak T e l e n g a C a r l 1 9 7 8 Hymenoptera: Ichneumonidae Hyposoter didymator ( T h u n b . ) C a r l 1 9 7 8

I s r a e l

Hymenoptera: Ichneumonidae Hyposoter didymator ( T h u n b . ) Rossler et al. 1975

E g y p t

Hymenoptera: Braconidae Apanteles s p p I b r a h i m 1 9 8 0 Microplitis rufiventris K o k I b r a h i m 1 9 8 0 Brecon brevicornis W e s m . I b r a h i m 1 9 8 0 Barylypa humeralis B r a u n s . I b r a h i m 1 9 8 0

USSR Hymenoptera: Braconidae Bracon brevicornis W e s m . H a b i b 1 9 7 3 Apanteles kazak T e l e n g a H a b i b 1 9 7 3 Hymenoptera: Trichogrammatidae Trichogramma evanescens W. H a b i b 1 9 7 3

South Africa

Hymenoptera: Braconidae Apanteles s p p H a b i b 1 9 7 3 Bracon brevicornis W e s m . C I B C 1 9 7 8 Cardiochiles nigricollis ( C a m . ) H a b i b 1 9 7 3 Hymenoptera: Ichneumonidae Charops s p p . H a b i b 1 9 7 3 Diptera: Tachinidae Palexorista laxa ( C u r r a n ) H a b i b 1 9 7 3 Goniophthalmus halli M e s n i l H a b i b 1 9 7 3

106 They found that the egg parasite, Trichogramma in the season, C. sonorensis may parasitize up to pretiosum Riley, and the larval parasite Microplitis 8 0 % of the H. virescens larvae in tobacco in North croceipes (Cresson) (= nigripennis A s h m e a d ) Carolina (A.H. Baumhover, Agricultural Research (Krombein et al. 1979) were the most frequently Service, U.S. Department of Agriculture, Oxford, encountered hymenopterans attacking H. zea in North Carolina, personal communication). Texas. They reported that M. croceipes, w h i c h w a s In Virginia, C. sonorensis (= Sagaritis provan- common in the fields late in the season, was cheri [Dalla Torre]) (Carlson 1972) parasitized responsible for lowering the H. zea larval p o p u l a • more than 50% of early-stage H. virescens larvae tions at that time of year. Although tachinids (Wene 1943). Other parasites that are distributed occurred, they were ineffective against large Helio• where Heliothis spp occur in the USA include Nete- this populations. lia, Winthemia, Hyposoter, a n d Meteorus species Surveys made in 1969 and 1970 of the parasites (Neunzig 1963; Shepard and Sterling 1972; Van of Heliothis spp in cotton in Texas by Shepard and den Bosch and Hagen 1966; Bottrell et al. 1968; Sterling (1972) showed that larval parasites Snow et al. 1966; A.H. Baumhover, personal accounted for approximately 7% regulation of Heli- communication). othis spp. They found that Cardiochiles nigriceps Vierick and Archytas marmoratus (Townsend) were most abundant, with Apanteles marginiventris Parasites Worldwide (Cresson), M. croceipes, a n d Eucelatoria bryani Sabrosky (= armiger [Coquillet]) (Sabrosky 1981) Extensive lists of parasites of H, armigera of the appearing less frequently; the egg parasite T. exi- world were given by Ibrahim (1980) and by Habib guum Pinto and Platner (= fasciatum [Perkins]) (1973); Ibrahim listed 103 species in 10 families of (Pinto et al. 1978) emerged from only 1 % of Helio- Hymenoptera and Diptera. A list of natural enemies this eggs collected. Van den Bosch and Hagen of Heliothis (armigera and assulta) in Taiwan was (1966) and Graham (1970) pointed out the impor- given by Yen (1973). In Egypt, Heliothis spp w e r e t a n c e of T. pretiosum Riley (= semifumatum [Per- parasitized predominantly by Apanteles spp, kins]) (Pinto et al. 1978) in Heliothis egg mortality in Microplitis rufiventris K o k „ Chelonus inanitus (L.), Texas and California. and to a lesser extent by Bracon brevicornis W e s m . Butler (1958a) reported that the only braconids a n d Barylypa humeralis Brauns (Ibrahim 1980, attacking Heliothis spp in Arizona were M. cro- 1981). ceipes a n d Chelonus insularis Cresson (= texanus Observations in India indicated that the parasites Cresson) (Krombein et al. 1979), while E. bryani that had an effect on H. armigera populations were (Butler 1958b) was the primary tachinid. In Okla- Campoletis chlorideae Uchida, the most important homa, the only important parasite of H. zea in cot- Heliothis parasite in India, Eriborus sp, Carcelia t o n w a s M. croceipes, while others common in H. illota (Curran) (=Eucarelia), Palexorista laxa (Cur- zea a n d H. virescens included C. insularis, E. ran) (=Drino imberbis [Wied.]) (CIBC 1978), Exo- bryani, Lespesia archippivora (Riley), and A. mar- rista fallax Mg., Goniophthalmus halli Mesnil a n d moratus (Bottrell et al. 1968; Young and Price Trichogramma spp, although 60 species of para• 1975). sites were recorded (Rao 1974). Campoletis chlori• In surveys by Snow et al. (1966) of Heliothis spp deae was imported to the USA from India, but larval populations on Geranium carolinianum L. in studies showed that this species adversely South Carolina, Mississippi, and Georgia, and in affected C. sonorensis populations in the field. cultivated and wild host plants by Lewis and Braz- When the two species mated, progeny had an zel (1968) and Smith et al. (1976a) in Mississippi, abnormal sex ratio. For this reason, it is not advis a • Cardiochiles nigriceps a n d M. croceipes w e r e ble to import C. chlorideae to countries where C. most common. However, C. nigriceps did not sonorensis already exists. d e v e l o p in H. zea. Roach's (1975) survey in north- Carl (1978) reported that Hyposoter didymator eastern South Carolina revealed that only C. nigri- (Thunb.) and Apanteles kazak Telenga were the ceps a n d Campoletis spp occurred in sufficient only important parasites of H. armigera f o u n d in numbers to affect Heliothis populations. Likewise in Greece and Bulgaria. These two species were to North Carolina, C. nigriceps a n d Campoletis sono- be shipped to New Zealand for testing of possible rensis Cameron were most commonly reared from interference with Apanteles ruficrus Hal. Heliothis spp in summer (Danks et al. 1979). Early The most abundant parasites of H. armigera in

107 Australia are t h e b r a c o n i d Microplitis demolitor Wil- Egypt (Ibrahim 1980). T h e most a b u n d a n t p r e d a • kinson a n d t h e i c h n e u m o n i d Heteropelma scapo- tors in cotton in Israel w e r e Chrysopa sp a n d Orius sum (Morley) ( M . S h e p a r d , C l e m s o n University, s p p (Rossler et al. 1975). India has five reduviids C l e m s o n , S o u t h Carolina, personal c o m m u n i c a - that attack Heliothis (Rao 1974), a n d one, Sycanus tion). I n o n e s o y b e a n field near C o o m i n y a , indagator (Stal), w a s i m p o r t e d to t h e U S A for study. Q u e e n s l a n d , m o r e t h a n 3 5 % of t h e Heliothis s p p Predation by S. indagator has b e e n studied by larvae w e r e parasitized by M. demolitor (Shepard, G r e e n e a n d S h e p a r d (1973) as well as others. L a w n a n d Schneider, in press). This s p e c i e s is A n o t h e r reduviid, Pristhesancus papuensis Stal, currently b e i n g investigated in t h e U S A for u s e in w a s i m p o r t e d f r o m Australia a n d studied in the m a n a g e m e n t p r o g r a m s for Heliothis. laboratory (Shepard, M c W h o r t e r , a n d King, in press). R o o m (1979) m a d e an extensive list of nat• ural e n e m i e s (predators a n d parasites) f o u n d in Predators Worldwide N a m o i Valley cotton in N e w South Wales, Australia. O t h e r studies in Australia ( B i s h o p a n d B l o o d 1981) C o m m o n predators on Heliothis in t h e USA are revealed that certain spider s p e c i e s exhibited listed in T a b l e 2. M a n y of t h e s e s a m e predator direct n u m e r i c a l relationships with c h a n g e s in Heli• g r o u p s w o r k against Heliothis spp in other parts of othis populations. T h e spiders' role in the natural t h e world. Coccinella, Scymnus, Orius, a n d Chrys- e n e m y c o m p l e x w a s c o n s i d e r e d important in r e g u • opa s p e c i e s w e r e a m o n g t h o s e predators listed for lating Heliothis.

T a b l e 2 . I m p o r t a n t p r e d a t o r s o f H e l i o t h i s s p p a n d s t a g e a t t a c k e d .

P r i n c i p a l P r e d a t o r s t a g e a t t a c k e d R e f e r e n c e

H e m i p t e r a Anthocoridae Orius insidiosus ( S a y ) E g g s L i n c o l n e t a l . 1 9 6 7 B e r y t i d a e Jalysus spinosus ( S a y ) E g g s E l s e y 1 9 7 2 L y g a e i d a e Geocoris punctipes ( S a y ) E g g s , f i r s t - s t a g e L o p e z e t a l . 1 9 7 6 ; l a r v a e L i n c o l n e t a l . 1 9 6 7 N a b i d a e Nabis s p p E g g s , f i r s t - , L i n c o l n e t a l . 1 9 6 7 ; second-stage D o n o h o e a n d P i t r e 1 9 7 7 l a r v a e Pentatornidae Podisus maculiventris ( S a y ) T h i r d - s t a g e l a r v a e L o p e z e t a l . 1 9 7 6

N e u r o p t e r a Chrysopidae Chrysopa carnea S t e p h e n s E g g s , f i r s t - s t a g e L o p e z e t a l . 1 9 7 6 l a r v a e

C o l e o p t e r a C a r a b i d a e Calosoma s p p L a r g e l a r v a e , L i n c o l n e t a l . 1 9 6 7 , v a n p u p a e d e n B o s c h & H a g e n 1 9 6 6 Calleida decora ( F . ) E g g s , s m a l l l a r v a e M . S h e p a r d , p e r s . c o m m . Coccinellidae Scymnus sp E g g s L i n c o l n e t a l . 1 9 6 7 Hippodamia convergens E g g s , f i r s t - s t a g e L i n c o l n e t a l . 1 9 6 7 (Guerin-Meneville) l a r v a e Coleomegilla maculate E g g s , f i r s t - , L i n c o l n e t a l . 1 9 6 7 ( D e G e e r ) second-stage l a r v a e

A r a n e i d a O x y o p i d a e Oxyopes salticus H e n t z Second-stage W h i t c o m b a n d E a s o n 1 9 6 7 l a r v a e

1 0 8 Increasing the Effectiveness of a n d 13 to 6 0 % of the first-stage larvae. Orius insidi- Naturally Occurring Predators osus (Say) was cited as o n e of the m o r e important predators. and Parasites In other field studies, Bell a n d W h i t c o m b (1964) a n d W h i t c o m b a n d Bell (1964) p l a c e d Heliothiszea Conservation of beneficial arthropods is a f u n d a • eggs on cotton plants and observed up to 4 5 % e g g mental principle of the integrated pest m a n a g e • predation. Van den B o s c h et al. (1969) d e t e r m i n e d ment (IPM) concept. Conservation is activity to that naturally occurring predators, particularly protect a n d maintain the pests' natural enemies, Geocoris pallens Stal, killed up to 6 6 % H. zea eggs i.e., reduction of activities that are deleterious to a n d first-stage larvae in field cages. t h e m . Perhaps the most important m e a n s of deal• Ewing a n d Ivy (1943) confined various predator ing with pest problems while c o n s e r v i n g natural species with H. zea eggs in the laboratory a n d e n e m i e s is to use selective control strategies, recorded the number c o n s u m e d . T h r e e predators, s o m e of these are host-plant resistance, selective Chrysopa rufilabris Burmeister, Hippodamia con- insecticides or judicious use of s o m e broad- vergens Guerin-Meneville, and Coleomegilla fusci- spectrum insecticides, and cultural practices. Suc• labris (Mulsant), c o n s u m e d over 25 eggs per cessful IPM programs include t h e s e a n d other predator per day. In other laboratory studies ecologically sound methods. B e c a u s e of t h e high (Lingren et al. 1968; Lopez et al. 1976) several value of cotton and t h e i m p o r t a n c e of Heliothis predator species w e r e efficient in c o n s u m i n g Heli• worldwide, m u c h of the research on natural e n e • othis eggs a n d larvae; the more voracious c o n • mies has b e e n c o n d u c t e d on this crop; c o n s e • s u m e d an average of 130 to 180 eggs a n d 1 0 4 to quently, m u c h of the following discussion relates to 136 larvae e a c h . Hippodamia convergens larvae cotton. c o n s u m e d large n u m b e r s of eggs, a n d adult females a n d Chrysopa spp larvae c o n s u m e d large n u m b e r s of first-stage Heliothis larvae. W h e n adult Geocoris punctipes (Say) and s e c o n d - s t a g e Faunal Diversity Chrysopa carnea Stephens larvae were confined to cotton terminals infested with H. virescens eggs Even in annually disrupted a g r o e c o s y s t e m s s u c h for 2 days, 78 to 8 8 % of the eggs were eaten. as cotton a n d maize, large n u m b e r s of predators Releases of predators in field c a g e s containing a n d parasites may be found. For example, in the immature Heliothis life stages demonstrate their USA, W h i t c o m b a n d Bell (1964) r e c o r d e d over 6 0 0 efficacy. Lingren et al. (1968) reported up to 9 9 % predators in Arkansas cotton fields, a n d V a n den reduction in H. virescens egg a n d larval popula• B o s c h a n d H a g e n (1966) estimated about 3 5 0 dif• tions after release of Chrysopa spp larvae alone, ferent predators and parasites in California. O n e of Geocoris spp adults alone, or a combination of both us (Smith) has estimated that 4 0 0 to 500 arthropod species. V a n den B o s c h et al. (1969) reported 41 to species are associated m o r e than superficially with 8 8 % reduction of H. zea after release of varying cotton fields in Mississippi. T h e diversity of paras• n u m b e r s of Geocoris spp, C. carnea, a n d Nabis ites was indicated earlier, a n d these tabulations did americolerus Carayon. not include parasites only occasionally r e c o r d e d attacking Heliothis. B a s e d on the previous data, Ridgway and Lingren (1972) surmised that 50 to 9 0 % of eggs a n d larvae of Heliothis are normally destroyed by naturally occurring predators a n d parasites. T h e y a g r e e d Natural Enemy Efficacy with Knipling (unpublished)' that it was reasonable to a s s u m e 7 5 % natural control of Heliothis by O n e of the first major studies on predators of Helio- insect predators a n d parasites for purposes of this w a s by Q u a i n t a n c e a n d Brues (1905). T h e y designing control programs. m a d e key observations on several p r e d a c e o u s e n e m i e s of H. zea in cotton a n d reported 5 1 % 1 parasitization of t h e larvae a n d 43 to 1 0 0 % parasiti- E.F. Knipling, 1967. A theoretical appraisal of the natural control agents in insect population dynamics and control with particular zation of e g g s in c o r n . Later, Fletcher a n d T h o m a s reference to Heliothis spp, unpublished report distributed to (1943) o b s e r v e d that during a 7-year period, preda• members of Entomology Research Division, U.S. Department of tors in the field destroyed 15 to 3 3 % of H. zea eggs Agriculture, December 13, 1967.4 pp.

109 Use of Insecticides b e t w e e n pest a n d beneficial species to any useful degree. However, "ecological" selectivity can be N e w s o m a n d Smith (1949) w e r e a m o n g t h e first t o effective. Early-planted trap plots or small plots of a recognize that insecticides could upset the interac• preferred plant c a n attract a n d c o n c e n t r a t e over- tion normally existing in untreated fields b e t w e e n wintered pest populations in small areas where aphids, spider mites, H. zea, and their natural ene• they can be treated with conventional insecticides, mies. R i d g w a y et al. (1 9 6 7) d e m o n s t r a t e d the thereby preserving the natural enemies in the impact of a p r e s u m a b l y selective insecticide, aldi- remainder of the field. carb, on predator populations, a n d the role of these predators in suppressing Heliolhis spp populations. O t h e r s h a v e also s h o w n the detrimental effect of Cultural Control insecticides on natural enemy populations. In fact, decline in predator populations in cotton Early workers used cultural practices as the main- fields has often b e e n attributed to insecticide appli• stay of their insect control efforts. Newsom (1975) c a t i o n s (Dinkins et al. 1970). However, Smith a n d pointed out that the rediscovery of the i m p o r t a n c e Stadelbacher (1978) reported that predator popu• of cultural control tactics—e.g., early planting, des- lations in c o t t o n within the Delta area of Mississippi truction of c r o p residues, a n d use of trap c r o p s - normally d e c l i n e in m i d - s e a s o n to late s e a s o n , has provided highly effective components of pest regardless of insecticide applications. They con• management systems for soybeans and cotton. cluded that peak predator populations closely T h e use of strip-cropping to increase beneficial c o i n c i d e d with peak squaring of cotton (Figure 1) arthropod populations was described by Laster a n d s u r m i s e d that plant phenology a n d attendant (1974). He pointed out that beef finishing on high- c h a n g e s in the nutritional value of the cotton plant energy silage has bee n introduced recently in the m a y explain the s e a s o n a l decline of natural Mississippi Delta, and this enterprise has potential e n e m i e s . for being c o m p a t i b l e with cotton production a n d for N e w s o m (1975) c o n c l u d e d that n o insecticides making good reservoir crops available for benefi- k n o w n then w e r e selective e n o u g h to discriminate cial insects. Robinson et al. (1972) found that cot-

C o m p o s i t e f i e l d

P r e d a t o r s

Bolls

20 40 6 0 80 100 1 2 0 1 4 0 160 180 2 0 0 M a y June J u l y A u g Sept O c t N o v

Figure 1. Rise and decline of predator populations within cotton fields in the Delta of Mississippi and correlation with Heliothis spp populations and plant phenology.

110 ton strip-planted with sorghum suffered less floral tion of thrips and aphid populations on seedling bud damage from bollworms than cotton strip- cotton through the widespread use of seeds planted with corn, soybean, alfalfa, or groundnut. treated with systemic insecticides and subsequent The importance of uncultivated marginal areas postplanting application of insecticides is bound to in the survival, buildup, and subsequent abun• be detrimental to the early-season establishment dance of predators and parasites in cotton cannot of these beneficials and their subsequent buildup in be overemphasized (Stadelbacher, unpublished cotton. data). Monoculture in modern agriculture, particu• larly of annual crops, often discriminates against natural enemies and favors development of "explo• Economic Thresholds, Decision sive" pest populations. Whitcomb (1974) stated Making, and Pest-Management that habitat manipulation both inside and outside the cultivated field will be emphasized in the future. Models He pointed out that the date of plowing, the specie s of plants on a highway right-of-way or canal bank, a drought, or even the destruction of the aphid popu• Economic Thresholds and lation on goldenrod by a fungus disease may affect Decision Making predator populations over a large area or lead to decisions on the number of insecticide applica• Control strategies for a pest-management system tions that must be used on nearby cultivated crops. are based on estimates of pest population densi• According to Fye (1972), management of naturally ties. The accuracy of these pest population esti• occurring populations of insect predators may mates depends on the reliability of the sampling depend on knowledge of the succession of winter methods. Thus, the dependability of economic weeds and crops that provide natural hosts for food thresholds (population levels at which supplemen• for the predator species. tal control measures are justified) that are used in In a 2-year study on the abundance of predators decision-making is subject to the quality of the in the various habitats in the Delta of Mississippi population estimates. Overestimation may result in between early March and mid-June, predator pop• unnecessary insecticide application or use of ulations in all the marginal areas except woods some other control measure that is not cost effec• margins were observed to be much higher than in tive (Gonzalez 1970). The need for economic thre• the more homogeneous areas, such as woods and shold data based on reliable pest population old cotton and soybean fields. The numbers of estimates is critical. With this information, growers beneficials found in the old cotton and soybean and farm advisors can be convinced more easily fields were proportional to the density of the stand that higher pest densities can be tolerated without a of winter and spring annuals, with soybean fields reduction in yield (Gonzalez 1970). haying the higher plant and predator populations Arthropod population levels have been deter• (E.A. Stadelbacher and J.W. Smith, Bioenviron- mined using two types of sampling procedures. mental Insect Control Laboratory, unpublished First, an estimate of the absolute population per unit data). The early-season activity of most predators area (Smith et al. 1976b) is used to study population in the Delta of Mississippi is very similar to that dynamics of pest and beneficial species in their reported by Whitcomb and Bell (1964) for Arkan• natural habitats. This information is useful in deter• sas. At that time, very few predators move directly mining thresholds and correlating the natural from overwintering sites to cotton; most emerge in enemy population with pest population dynamics. March and early April and pass one or two genera• The potential effect of natural enemies on Helio- tions on weeds and legumes in the uncultivated this spp populations is often recognized in insect marginal areas. control guides, but explicit instructions for using The maturation of early-season host plants and their numbers in decision-making are generally dispersal of natural enemies normally is well syn• lacking, and where present, are used with reserva• chronized with the germination and early develop• tions. Numbers of naturally occurring predators ment of cotton. Numerous ingenious methods have can be used in decision-making, as shown by Hart- been tested to entice, force, release, feed, hold, a n d stack et al. (1976). They describe an index whereby manipulate natural enemy populations to increase a predator: prey ratio is established, and the prob a • their abundance in cotton fields. However, elimina- bility of biological control occurring is predicted

111 (Figure 2). As egg density on the vertical axis enemy populations. Research in each of these increases, the necessity of intervention becomes areas is important for effective Heliothis more urgent, depending on the predator population management. given on the horizontal axis. In the "Treat" region of the figure, the probability of biological control occurring is low because of low predator numbers. Pest-Management Models In the region between the dotted lines, the effec• tiveness of biological control is uncertain; there• An emerging technology used in planning and exe• fore, other factors (weather, plant phenology, etc.) cuting pest-management strategies consists of may be important in making a treatment decision. computer-oriented, weather-based simulations of Finally, in the lower region a high predator: prey agricultural production systems. The development ratio exists, with a consequent high probability that and use of these models require the coordinated biological control will o c c u r . efforts of multidisciplinary teams. Accurate economic thresholds must be estab• The main controlling factors for the functions in lished for each crop and cotton-growing area, and each life stage in each generation of an insect further decision-making techniques must contain should be understood for development of realistic the flexibility to account for season, plant maturity, models. Some of these dependent functions are: weather, and treatment history as well as natural rates of development and egg production, mating behavior, egg fertilization, longevity, mortality, migration, diapause, host selection, and feeding behavior. Much emphasis will be placed on the 125 interactions of these factors in pest-management systems models in the immediate future. For exam• ple, one cotton model, which is a modification of Undecided... SIMCOTT II (McKinion et al. 1974), incorporates a check field Heliothis spp submodel and predation and parasit• 100 populations ism subsubmodels (Hartstack et al, 1976). Other a g a i n Heliothis models that might fit equally well in the T r e a t 1 o r 2 future are being developed in the USA (Arizona, d a y s California, Mississippi, and North Carolina).

7 5 Natural mortality such as predation has been considered in several Heliothis spp models. An example of one approach used at Mississippi State University was developed specifically for interfac• ing with COTCROP and BWEEV. Since H. zea a n d 50 H. virescens develop and oviposit at different rates, and also react differently to insecticides, they are separated in this model. The model further separ• D o n o t ates H. virescens by cohorts (insects that enter a t r e a t life stage on the same day). The variance in devel• 2 5 opment time within a cohort is accounted for by movement of the members of a cohort to the next life stage distributed over several days. The stage is a function of the age of the cohort and the degr e e day (temperature) accumulation for that day. 10 20 30 40 50 60 Fecundity is a function of temperature and moth 1 0 0 0 ages. The number of eggs destroyed daily by pre• dators is calculated and the proportion of the larvae No. of effective predators within each cohort that are destroyed by the preda• tors varies with the age of the cohort. Figure 2. Decision-making index (utilizing pre• dator: prey ratio) based on the probability of Another approach to handling predation in Helio• biological control occurring (Source: Hartstack this spp models is that of Knipling and McGuire et al. 1976). (1968). These simple models were adapted by

112 Hartstack et al. (1976) in their Heliothis m o d e l but results are often inconsistent, and economic M O T H Z V - 2 : feasibility is generally lacking. The difficulty of mass producing natural enemies at a cost compet• M = 1-EXP [(-0.693) (Pn)/(N) (S)] itive with other control strategies is a major factor limiting use of the augmentation strategy. Thus, w h e r e emphasi s has been p l a c e d on Trichogramma spp M = probability of egg or larval mortality; a n d Chrysopa spp because these two natural ene• Pn = number of effective predators; mies can be mass produced (see Morrison et al. N = number of Pn to cause 50% mortality; a n d 1978, Shcheptil'nikova et al. 1974, and Jiminez S = relative search area. 1980 for Trichogramma spp; Ridgway and Vinson 1977 for Chrysopa carnea). The following is a brief Other factors that influence predation can be review of progress made within the last 15 years on assessed in a similar manner. The exponential the use of selected natural enemies for biological functions are only a suggestion from A.W. Hart- control of Heliothis spp by augmentation. stack, (College Station, Texas, personal communi• cation), and he stated that other types of functions Trichogramma Spp may fit the data better. Both of the above approaches are in use at present, each with certain Tests demonstrating increase in parasitization advantages. These models and submodels would after release of Trichogramma spp are given in fit into a system model that could be used in area- Table 3. Some of the tests in cotton indicated a w i d e programs to guide farmers in their decisions reduction in larval population as a consequence of on application of insect pest management parasitization. However, only in tests with tomatoes techniques. was yield correlated with increased parasitization. In the USA, the following major advances have been made in the taxonomy and production and Biological Control by Augmenting utilization of Trichogramma: Natural Enemy Populations 1. The taxonomy of North American species has recently been placed on a solid foundation with the designation of neotypes for T. pretiosum a n d T. Production, Release, and Evaluation minutum and the designation of lectotypes for sev• eral species often confused in the past literature The possibility of augmenting natural enemies to (Pinto et al. 1978). obtain control of arthropod pests has been consi• dered. Results of early efforts have been summar• 2. Host eggs are "glued" to a permanent substrate ized by Clausen (1956) and DeBach and Hagen with a fine mist of water for exposure to the paras• (1964). More recently, a book edited by Ridgway ites, thereby making the parasitized eggs available and Vinson (1977) reviewed biological control by in free form for distribution (Morrison et al. 1978). augmentation of natural enemies, worldwide, including theoretical aspects as well as production 3. T h e quality of T. pretiosum reared on Sitotroga and utilization. Other general reviews include Rabb cerealella (Olivier) eggs is assured by use of a et al. (1976) and Stinner (1977). Specifically, Kni - broad genetic base and rearing hosts on wheat pling (1979) developed theoretical models for containing at least 13% protein (King and Morrison, appraising the potential value of augmentative in press). releases of predators a n d parasites a n d Ridgway et al. (1981) reviewed the use of Trichogramma spp in 4. A mechanical unit has been designed and con• augmentative releases to control lepidopterous structed for aerial broadcast application of parasit• pests. King and Morrison (in press) reviewed pro• ized host eggs under refrigerated conditions duction of predators and parasites, including qual• (Bouse et al. 1981). ity control and in vitro rearing.

The technical feasibility of suppressing Heliothis 5. The role that host-seeking substances play in spp by augmenting parasite and predator popula- aiding parasites and predators to find their hosts tions has been demonstrated (Tables 3, 4, and 5), has b e e n elucidated.

1 1 3 Table 3. Biological control of Heliothis spp by augmentative release of Trichogramma.

Release No. of Parasitization (%) rate eggs Release NonreIeased Heliothis spp (000/ha)a ( 0 0 0 / h a ) (treated) or prereleased Control evidence Reference

Cotton

H. zea/H. virescens 494.0 58 11 Lingren and Kim 1970 46.0-955.9 7.4-27.7 33-81 5 Stinner et a l . 1974 191.4 297.1 7.4-27.7 6 1 7 6 6 % reduction in Heliothis l a r v a e Stinner e t a l . 1974 123.5-247.0 24-73 0-7 Ridgway et a l . 1977 176.0 0.2- 7.8 0-43 3-27 J o n e s e t a l . 1977 176.0 6.0-39.3 3-73 0- 9 J o n e s et a l . 1977 112.0-178.0 14.6-17.1 55-84 7-81 2 1 % reduction in Heliothis larvae J o n e s e t a l . 1979b. 110.0 15-90 15-90 Reduction in Heliothis larvae A b i e s e t a l . 1979b

Tomato

H. zea 40.5 81 75 45% reduction in f r u i t damage Oatman and Platner 1971 49.6 64 42 7 1 % reduction i n f r u i t damage Oalman and Platner 1971 74.1-98.8 53-85 0-41 84% reduction in f r u i t damage Oatman and Platner 1971

H. armigera 125.0 35 6 Patel 1975 250.0 71 26 65% reduction in f r u i t damage Patel 1975 250.0 76 2 69% reduction in f r u i t damage Patel 1975 a . Releases typically made at 2- to 4-day intervals for several applications, except for Patel 1975. where rel e a s e s w e r e m a d e a t 7 - t o 1 0 - d a y i n t e r v a l s . b . Releases conducted using latest taxonomic, rearing, a n d r e l e a s e t e c h n o l o g y . Table 4. Biological control of H . z e a a n d H. virescens In cotton by augmentative release of C. carnes.a

N o . H. zea a n d H. virescens l a r v a e / h a

N o . o f C . c a r n e a R e l e a s e N o n r e l e a s e L a r v a l C a g e o r r e l e a s e d ( t r e a t e d ) ( c o n t r o l ) r e d u c t i o n f i e l d t e s t ( 0 0 0 / h a ) (%)

1 0 3 7 . 0 1 . 5 4 2 . 0 9 6 C a g e 9 8 8 . 0 0 . 7 1 4 4 . 7 9 9 C a g e 9 8 8 . 0 3 5 . 6 1 4 4 . 7 7 5 C a g e 6 1 . 8 4 . 0 1 5 . 1 7 4 C a g e 2 4 7 . 0 4 . 0 1 5 . 1 7 4 C a g e 7 4 1 . 0 4 . 0 1 5 . 1 9 0 C a g e 3 6 0 . 6 1 . 7 4 4 . 5 9 6 C a g e 4 9 4 . 0 4 . 2 2 3 . 5 8 2 F i e l d 2 2 7 . 2 2 . 0 1 8 . 5 8 9 F i e l d 2 4 . 7 1 0 . 4 1 5 . 6 3 3 F i e l d 7 4 . 1 7 . 2 1 5 . 6 5 4 F i e l d 2 4 7 . 0 2 . 7 1 5 . 6 8 3 F i e l d

a . S o u r c e : R i d g w a y e t a l . ( 1 9 7 7 ) .

Table 5. Parasitism on Heliothis spp in cages afterr release of larval parasites.

N o . o f N o . o f Heliothis P a r a s i t i s m P a r a s i t e parasites/ha l a r v a e / h a (%) R e f e r e n c e

Campoletis sonorensis 1 9 9 3 1 1 1 1 5 5 2 Noble and Graham 1 9 6 6 C. sonorensis 3 9 8 4 2 1 2 4 2 8 2 Noble and Graham 1 9 6 6 C. sonorensis 2 0 6 2 8 5 - 9 5 Lingren 1977 Microplitis croceipes 2 9 6 4 5 8 Jackson et al.1970 Eucelatoria sp 6 1 7 5 4 5 7 0 5 7 Jackson et al.1970 Palexorista laxa 6 1 7 5 3 2 7 3 5 1 Jackson et al.1970

Tests combining this technology are footnoted in releases for the third generation) resulted in Table 3. In addition, a pilot study is being conduc t e d increased parasitism, reduced Heliothis larvae per in southeast Arkansas, USA (1980-1983), to con• 100 plants, and reduced damage to floral buds and solidate this technology into a scheme for the use bolls. of Trichogramma as an effective and acceptable pest-management alternative. Other reports on use of Trichogramma for control of Heliothis spp by Predators augmentative release are Beglyarov and Smetnick (1977) and Bournier and Peyrelongue (1973). No predators are currently being used to any Wang (1979) provides directions for the use-of degree for controlling Heliothis spp by augmenta• Trichogramma to control Heliothis in cotton in tion. However, Ridgway and his coworkers have China. Release of Trichogramma at the rate of 227 demonstrated the technical feasibility of suppress• thousand/ha (five releases for the second genera• ing Heliothis spp larval populations in cotton by tion of Heliothis) and 303 thousand/ha (three periodic release of C. camea eggs or larvae (Table

115 4). In fact, release of 2- to 3-day-old larvae consist• releases has been indicated in some small-scale ently produced significant reductions of Heliothis tests (Table 5), and Knipling (1979) demonstrated spp on cotton. Reductions in Heliothis spp larval in theoretical studies the feasibility of suppressi n g populations were obtained by releasing as few as Heliothis spp populations areawide by augmenta• 24.7 thousand C. carnea larvae/ha, and high levels tive releases. of reduction were obtained in the field by releasing Lingren (1969) reported that A. marginiventris 247 to 494 thousand/ha (Ridgway et al. 1977). had considerable potential for use in augmentation Releases of several hemipteran predators indi• programs. Also, release of C. sonorensis at the rate cate that it might be feasible to augment their pop u • of 680 per day for 10 consecutive days in a 0.2 ha lations if economical procedures for mass cage infested with H. virescens resulted in 85% producing them could be developed. Field-cage parasitization for 9 consecutive weeks (Lingren studies by Lingren et al. (1968), Van den Bosch et 1977). Jackson et al. (1970) reported 58% parasiti• al. (1969), and Lopez et al. (1976) with G. punctipes, zation of third-stage H. virescens larvae in cages N. americoferus, a n d Podisus maculiventris Say, when 2964 (equivalent) M. croceipes (Cresson) respectively, in cotton demonstrate the ability of female wasps were released per ha. Jackson et al. these predators to suppress Heliothis spp popula- (1970) reported from their studies with tachinids tions. Another hemipteran predator, Jalysus spino- that if Eucelatoria bryani a n d Palexorista laxa (a sus (Say), has been used experimentally in parasite imported from India) were released at the tobacco to suppress populations of H. virescens rate of 6175 female flies per ha on cotton contain• a n d Manduca sexta. In one experiment, the sea• ing 12 3 5 0 Heliothis spp larvae per ha, about 50% sonal density of J. spinosus was increased by parasitization should occur in 2 days. early-season releases, but only Manduca spp w e r e The tachinids above can only be considered as suppressed (Elsey 1975). population suppressants, since they prefer late- Gillaspy (1979) reviewed the possibility of man• stage larvae; consequently they cause little direct aging lepidopterous pest populations by use of reduction in damage (Brewer and King 1980). Polistes wasps. He described shelters that could However, the solitary hymenopterous parasites be easily erected and dismantled for use around prefer second- to third-stage larvae and directly target fields as nesting areas for the wasps. His reduce crop damage by reducing larval food con• studies, as well as a number of others that he cited, sumption after parasitization. indicated that these wasps are opportunistic and Larval parasites are typically strong fliers and will attack prey (lepidopterous larvae) that are most disperse, thus making it difficult to assess their readily available, including Heliothis spp. Others efficiency in cage studies. In one field study, Lew i s have also reported research on the use of Polistes et al. (1972) reported that 80% parasitism of H. spp as possible control agents for Heliothis spp. For virescens larvae in cotton could be attained with example, Lawson et al. (1961) reported on control 988 to 1482 C. nigriceps females per ha. Their in tobacco fields, and the Institute of Agricultural calculations were based on a 2-year study during and Forestry Sciences of Shang-Chiu (1976) which visual estimates of total actively searching reported that Polistes spp could be used for insect f e m a l e s of C. nigriceps per ha were made and pest control in cotton fields. This latter report stated correlated with percentage of H. virescens larvae that Polistes spp, when introduced in colonies of parasitized by C. nigriceps. Similar studies need to about 1500 wasps per ha, are effective in control• be conducted on other larval parasite species. ling H. armigera and another lepidopterous spe• cies. The report also stated that a control rate of about 70 to 80% larval reduction could be attained Nutrition, In Vitro Rearing, and Quality 5 to 7 days after nest transfer. Control

Artificial diets have been developed for C. carnea, Larval Parasites though improvement is still needed (King and Mor• rison, in press), and diets have been developed for As stated earlier in this paper, larval parasites are in vitro rearing of several parasites, including Tri- an important factor in the environmental resistance chogramma (King 1981). Consistent and economi• against increases in Heliothis spp populations. cal production of quality natural enemies for use in Potential for using larval parasites in augmentativ e augmentation programs may well depend on con-

116 tinued advancement in our knowledge about nutri• et al. 1981). Here, the chemistry of substances tional requirements of predators and the found in moth scales that elicit activity by Tricho• development of in vitro rearing techniques for gramma spp, and in larval frass, cuticle, and/or parasites. salivary glands, that elicit response by hymenop- Opportunities exist for improving the quality of terous and tachinid larval parasites, is discussed. mass-produced natural enemies by reduction of As part of a pilot study, diatomaceous earth parti• genetic deterioration and by improved nutrition. cles are being impregnated with crude extracts of However, techniques must first be developed for H. zea moth scales and applied along with sterile H. monitoring the essential characteristics. At pres• zea eggs to retain and increase the effectiveness of ent, genetic deterioration in C. camea a n d Tricho- aerially applied T. pretiosum. Substantial informa• gramma spp is partially circumvented by tion exists in support of the possibility that kairo• periodically replacing the laboratory colony with mones can eventually be used to manipulate the field-collected material. Vigor is maintained in Tri- field behavior of Heliothis spp parasites and chogramma colonies in the People's Republic of predators. China by requiring them to fly in search of host eggs (King and Morrison, in press). Parasite quality may be dependent on nutrition of the host, and as stated Discussion earlier, wheat containing below 13% protein con• tent is unacceptable for rearing the unnatural host, Heliothis spp are among the most economically S. cerealella, for production of Trichogramma. important insects of cultivated crops worldwide, Genetic deterioration or reduced quality may be even though they are attacked by a wide range of indicated by changes in natural enemy adaptabil• natural enemies. Vacant niches (e.g., unattacked ity, sexual activity, host selection, and/or motility. life stages of Heliothis spp or host plants that are unattractive to indigenous natural enemies) do occur, and opportunities exist for establishing mor e Management of Parasites and Predators effective natural enemies. Considering the eco• nomic importance of species such as H. zea a n d H. Dispersal from the target area after release often armigera, establishment of even a partially effec• reduces the effectiveness of the augmentation tive natural enemy against a particular life stage approach. Provision of supplemental resources could result in saving millions of dollars as well as such as food to maintain the released or indigen• reducing environmental pollution from insecti• ous natural enemy, and use of kairomones to cides. Some effort should be made toward explora• attract, arrest, retain, or stimulate the natural tion, importation, and establishment of natural enemy to search more intensively for the host or enemies that have been shown to regulate Helio• prey could provide mechanisms for managing par• this spp populations. asites and predators (Hagen and Hale 1974; Nord- Indirectly, most economic thresholds for Helio- lund et al. 1981). this spp on crops include suppression by natural Ables and Ridgway (in press) reviewed the use of enemies, and insect control guides often refer to supplementary foods, particularly simulation of the need tor preserving predators and parasites of aphid honeydew to attract and concentrate adult Heliothis. However, explicit instructions for moni• chrysopid populations. Hagen et al. (1971) toring and using natural enemy numbers in actual reported that a dairy product composed of the decision-making are generally lacking. Thus, the yeast Saccharomyces fragilis and its whey sub• efficacy of key predators and parasites should be strate sprayed on cotton increased the effective• determined through the use of correlative and ness of C. carnea against H. zea eggs and larvae. experimental methods (day and night observa• Coccinellid populations have also been reported to tions); means must be developed for rapidly moni• be increased in response to application of supple• toring these populations so that their numbers can mentary foods such as sucrose or molasses on be used in decision-making; and dynamic eco• com plants (Carlson and Chiang 1973). nomic thresholds for Heliothis should be developed The "state of the art" in identification, elucidation that include natural enemy numbers (qualitatively of the role of, and utilization of chemicals (kairo• and quantitatively weighted). mones) that aid parasites and predators in finding Research must be continued on the develop• their hosts has recently been reviewed (Nordlund, ment of selective insecticides for Heliothis s p p as

117 well as other associated pest insects. Insecticidal A C H A N , P . D . , M A T H U R , K . C . , D H A R M A D H I K A R I , intervention will continue to be necessary on many P.R., and M A N J U N A T H , T . M . 1 9 6 8 . Parasites of Helio• crops, regardless of advances in host-plant resist• this s p p . in India. P a g e s 1 2 9 - 1 4 9 in C o m m o n w e a l t h Insti• ance and biological control. Thus, sound economic tute of Biological Control technical bulletin 10, Ascot , B e r k s , U K . thresholds are required so that chemicals can be

used only as needed, and application techniques B E G L Y A R O V , G . A . , a n d S M E T N I K , A . I . 1 9 7 7 . S e a • should allow for maximum predator and parasite sonal colonization of entomophages. In Biological control survival. b y a u g m e n t a t i o n o f n a t u r a l e n e m i e s , e d s . R.L. R i d g w a y

The ability to consistently control Heliothis spp a n d S.B. V i n s o n . N e w Y o r k , USA: P l e n u m . 4 8 0 pp.

by augmentative release of predators and/or par- B E L L , K . O . , a n d W H I T C O M B , W . H . 1 9 6 4 . Field s t u d i e s asites, at a cost competitive with the use of insecti- on e g g p r e d a t o r s of t h e b o l l w o r m , Heliothis zea ( B o d d i e ) . cides, is dependent on (1) elucidation of factors Florida E n t o m o l o g i s t 4 7 : 1 7 1 - 1 8 0 . affecting host searching and (2) development of B I S H O P , A . L , a n d B L O O D , P . R . B . 1 9 8 1 . Interactions mass-production procedures using artificial diets. between natural populations of spiders and pests in cot • Even in the case of Trichogramma, in vitro rearing t o n a n d their i m p o r t a n c e t o c o t t o n p r o d u c t i o n i n s o u t h - techniques utilizing defined artificial diets could eastern Queensland. General Applied Entomology enable production of a high-quality, standardized 1 3 : 9 8 - 1 0 4 . product. In fact, the present cost of rearing Tricho• B O T T R E L L , D . G . , Y O U N G , J . H . , P R I C E , R . G . , and gramma is U.S. $0.03 to $0.05 per 1000, and of C. A D A M S , R . H . 1 9 6 8 . Parasites reared from Heliothis s p p . carnea is U.S. $1.50 to $2.50 per 1000 (R.K. Morri• in O k l a h o m a in 1 9 6 5 a n d 1 9 6 6 . A n n a l s of t h e E n t o m o l o g i • son, Cotton Insect Research Unit, ARS, U.S. cal Society of America 61:1053-1055. Department of Agriculture, College Station, Texas, B O U R N I E R , J . P . , a n d P E Y R E L O N G U E , J . Y . personal communication). Additionally, efforts 1 9 7 3 . I n t r o d u c t i o n , e l e v a g e et l a c h e r s de Trichogramma should be intensified to isolate and identify chemi• brasiliensis A s h m . ( H y m . C h a l c i d i d a e ) en v u e de lutter cals emanating from the host, host products, and c o n t r e Heliothis armigera H b n . ( L e p . N o c t u i d a e ) a M a d a • plant that can be used to manage natural enemies g a s c a r . C o t o n e t Fi b re s T r o p i c a l e 28:231 - 2 3 7 . of the pest, particularly in augmentative releases. B O U S E , L.F., C A R L T O N , J . B . , a n d M O R R I S O N , R.K. International cooperation could encourage the 1 9 8 1 . A e r i a l a p p l i c a t i o n o f insect e g g parasites. T r a n • flow of information on biological control of Heliothis sactions of the American Society of Agricultural Engi• as well as the exchange of natural enemies. Spe- neers 1981: 1093-1098. cific natural enemies occur only at particular times B R A Z Z E L , J.R., N E W S O M , L.D., R O U S S E L , J . S . , of the season, and this, coupled with travel restric- L I N C O L N , C , W I L L I A M S , F.J., and B A R N E S , G . tions, often prohibits the importation of important 1 9 5 3 . Bollworm and tobacco budworm as cotton pests in natural enemies. Also, international cooperation Louisiana and Arkansas. Louisiana Agricultural Experi• could enable rapid screening of candidates for m e n t S t a t i o n t e c h n i c a l bulletin 4 8 2 , B a t o n R o u g e . L a , identification and augmentation of those that can U S A . 4 7 p p . be most easily mass reared and managed after B R E W E R , F . D . , a n d K I N G , E . G . 1 9 8 0 . Consumption release. a n d utilization of a s o y f l o u r - w h e a t g e r m diet by larvae of t h e t o b a c c o b u d w o r m p a r a s i t i z e d by t h e t a c h i n i d Eucela- toria sp. E n t o m o p h a g a 2 5 ( 1 ) : 9 5 - 1 0 1 . References B U T L E R , G . D . , Jr. 1 9 5 8 a . B r a c o n i d w a s p s r e a r e d f r o m

A B L E S , J.R., J O N E S , S.L., M O R R I S O N , R.K., lepidopterous larvae in Arizona. Pan-Pacific Entomolog i s t H O U S E , V . S . , B U L L , D.L., B O U S E , I.F., a n d C A R L - 34-222-223. T O N , J . B . 1 9 7 9 . N e w d e v e l o p m e n t s i n t h e u s e o f Tricho• B U T L E R , G . D . , Jr. 1958b. T a c h i n i d flies r e a r e d f r o m gramma to c o n t r o l l e p i d o p t e r a n p e s t s of c o t t o n . P a g e s l e p i d o p t e r o u s larvae i n A r i z o n a , 1 9 5 7 . J o u r n a l o f E c o • 1 2 5 - 1 2 7 in P r o c e e d i n g s , B e l t w i d e C o t t o n P r o d u c t i o n nomic Entomology 51:561 -562. Research Conference, National Cotton Council, 1979, M e m p h i s , T e n n , U S A . CIBC (Commonwealth Institute of Biological Con• t r o l ) . 1 9 7 8 . Possibilities of biological control of Heliothis A B L E S , J . R . , a n d R I D G W A Y , R.L. 1 9 8 2 . Augmentation armigera a n d H. zea. CIBC status paper 13, Ascot, Berks, of entomophagous arthropods to control pest insecis an d UK. m i t e s . P a g e s 1 0 3 - 1 2 7 in Proceedings, Symposium in Agricultural Research. V. Biological control in crop pr o • C A R L , K.P. 1 9 7 8 . Heliothis armigera; p a r a s i t e s u r v e y d u c t i o n , Beltsville, U S A . a n d i n t r o d u c t i o n of Apanteles kazak to N e w Z e a l a n d .

118 Commonweath Institute of Biological Control Report, Conference on Ecological Animal Control by Habitat European Station, Delemont, Switzerland. 8 pp. Management, 26-28 Feb 1970, Tallahassee, Fla, USA.

CARLSON, R.W. 1972. Suppression of the name Cam- GRAHAM, H.M. 1970. Parasitism of eggs of bollworms, poletis perdistincta (Hymenoptera: Ichneumonidae) and tobacco budworms and loopers by Trichogramma semi- the identity of species to which the name has been a p • fumatum in the Lower Rio Grande Valley, Texas. Journal plied. Entomological News 93:75-82. of Economic Entomology 63:686-688.

CARLSON, R.E., and CHIANG, H.C. 1973. R e d u c t i o n GREENE, G.T., and SHEPARD, M. 1973. Biological of an Ostrinia nubilalis population by predatory insects studies of a predator, Sycanus indagator. II. Field survival attracted by sucrose sprays. Entomophaga 18:205-211 . and predation potential. Florida Agricultural Exper i m e n t Station Journal Series No. 5002. 38 pp. CLAUSEN, C.P. 1956. Biological control of insect pests HABIB, R. 1973. Memorandum on possibilities of biolog• in the continental United States. U.S. Department of A g r i • ical control of Heliothis armigera. Commonwealth Insti• culture technical bulletin 1139, Washington DC, USA . 151 tute of Biological Control, Rawalpindi, Pakistan. 18 p p . PP HAFEZ, M. 1951. Notes on the introduction and biology COMMON, I.F.B. 1953. The Australian species of Heli- of Microplitis demolitor Wilk. Bulletin of the Society of othis and their pest status. Australian Journal of Zoolo g y Fouad ler Entomology 35:107-120. 1:319-344. HAGEN, K.S., and HALE, R. 1974. Increasing natural DANKS, H.V., RABB, R.L., and SOUTHERN, P.S. enemies through use of supplementary feeding and no n - 1 9 7 9 . Biology of insect parasites of Heliothis larvae in target prey Pages 170-181 in Proceedings, Summer North Carolina. Journal of the Georgia Entomologica l Institute on Biological Control of Plant Insects an d D i s • Society 14:36-64. eases, eds. F.G. Maxwell and F.A. Harris. Jackson, Miss, DeBACH, P., and HAGEN, K.S. 1964. Manipulation of USA: University Press of Mississippi. 647 pp. entomophagous species. Pages 429-458 in Biological HAGEN, K.S., SAVELL, E.F., Jr., and TASSAN, R.L. control of insects, pests and weeds, ed. P. DeBach. L o n • 1 9 7 1 . The use of food sprays to increase the effective• don, UK: Chapman and Hall. ness of entomophagous insects. Proceedings, Tall DINKINS, R.L., BRAZZEL, J.R., and WILSON, C.A. Timbers Conference on Ecological Animal Control by 1 9 7 0 . Seasonal incidence of major predaceous arthro• Habitat Management 2:59-81. pods in Mississippi cotton fields. Journal of Econo m i c HALLMAN, G. 1980. Revista Columbiana de entomolo- Entomology 63:814-817. gia publicacion oficial de la sociedad Columbiana de

DONOHOE, M.C., and PITRE, H.N. 1977. Reduviolus entomologia. September 1980. 4 (3 and 4): 60-69. roseipennis behavior and effectiveness in reducing HARDWICK, D.F. 1965. The corn earworm complex. n u m b e r s of Heliothis zea on cotton. Environmental Ento• Memoirs of the Entomological Society of Canada 40, mology 6:872-876. Ottawa, Canada. 247 pp.

ELSEY.K.D.1972. Predation of eggs of Heliothis spp. on HARDWICK, D.F. 1970. A generic revision of the North tobacco. Environmental Entomology 1:433-438. American Heliothidinae (Lepidoptera: Noctuidae). Memoirs of the Entomological Society of Canada 73, ELSEY, K.D. 1975. Jalysus spinosus: I n c r e a s e d Ottawa, Canada. 59 pp. numbers produced on tobacco by early season releases. Tobacco Science 19:13-15. HARTSTACK, A.W., Jr., WITZ, J.A., HOLLINGS- WORTH, J.P., RIDGWAY, R.L., and LOPEZ, J.D. EWING, K.P., and IVY, E.E. 1943. Some factors 1976. MOTHZV-2: a computer simulation of Heliothiszea influencing bollworm populations and damage. Journa l o f a n d Heliothis virescens population dynamics. U.S. Economic Entomology 36:602-606. Department of Agriculture User's Manual ARS-S-127, FLETCHER, R.K., and THOMAS, F.L. 1943. N a t u r a l Washington DC, USA. 55 pp. control of eggs and first instar larvae of Heliothis armig- IBRAHIM, A.E. 1980. Biotic factors affecting different era. Journal of Economic Entomlogy 36:557-560. species in the genera Heliothis a n d Spodoptera in Egypt. FYE, R.E. 1972. The interchange of insect parasites and Institute of Plant Protection Report 2, Cairo, Egypt. 56 p p . predators between crops. Pest Articles and News Sum • IBRAHIM, A.E. 1981. Biotic factors affecting different maries 18:143-146. species in the genera Heliothis a n d Spodoptera in Egypt.

GILLASPY, J.E. 1979. Management of Polistes w a s p s Institute of Plant Protection, Report 4, Cairo, Egypt. 58 p p . for caterpillar predation. Southwest Entomologist 4 : 3 3 4 - Institute of Agricultural and Forestry Sciences of 3 5 2 . Shang-Chiu. 1976. A preliminary study on the bionom•

GONZALEZ, D. 1970. Sampling as a basis for pest ics of hunting wasps and their utilization in cotto n i n s e c t management strategies, in Proceedings, Tall Timbers control. Acta Entomologica Sinica 19:303-308.

1 1 9 JACKSON, C.G., BRYAN, D.E., BUTLER, G.D., Jr., and F.A. Harris. Jackson, Miss, USA: University Pres s of and PATONA, R. 1970. Development, fecundity, and M i s s i s s i p p i . 6 4 7 p p . longevity of Leschenaultia adusta, a t a c h i n i d p a r a s i t e of LAWSON, F.R., RABB, R.L., GUTHRIE F.E., and the salt marsh caterpillar. Journal of Economic Entom o l • BOWERY, T.G. 1961. Studies of an integrated control ogy 63:1396-1397. system for hornworms on tobacco. Journal of Economic JIMINEZ, E. 1980. Review of some interesting develop• Entomology 54:93-97. ments, (3.2) plant protection, Mexico. International LEA, A.M. 1928. T h e c o t t o n b o l l w o r m i n S o u t h Australia. Organization of Biological Control Newsletter 15:5. Journal of Agriculture South Australia 31:608-615. JONES. S.L., MORRISON, R.K., ABLES, J.R., and LEWIS, W.J., and BRAZZEL, J.R. 1968. A three-year BULL, D.L. 1977. A n e w a n d i m p r o v e d t e c h n i q u e for t h e s t u d y o f p a r a s i t e s o f t h e b o l l w o r m a n d t h e t o b a c c o b u d - field r e l e a s e of Trichogramma pretiosum. Southwestern worm in Mississippi. Journal of Economic Entomology Entomologist 2:210-215. 61 ; 6 7 3 - 6 7 6 . JONES, S.L., MORRISON, R.K., ABLES, J.R., LEWIS, W.J., SPARKS, A.N., JONES, R.L., and BAR- BOUSE, L.F., CARLTON. J.B., and BULL, D.L. RAS, D.J. 1972. Efficiency of Cardiochiles nigriceps as a 1 9 7 9 . New techniques for the aerial releases of Tricho• p a r a s i t e of Heliothis virescens on cotton. Environmental gramma pretiosum. Southwestern Entomologist 4:14-19. Entomology 1:468-471. KING, E.G., Jr. 1981. Production, release, and evalua• tion of predators and parasites of arthropod pests att a c k • LINCOLN, C., PHILLIPS, J.R., WHITCOMB, W.H., ing f o o d a n d fiber c r o p s in the U S A . P a g e s 1 5 4 - 1 6 8 in POWELL, G.C., BOYER, W.P., BELL, K.O., Jr., DEAN, Proceedings, First Japan/USA Symposium on IPM 29-30 G.L., MATTHEWS, E.J., GRAVES, J.B., NEWSOM, Sept 1981, Tsukuba, Japan. L.D., CLOWER, D.F., BRADLEY, J.R., Jr., and BAGENT, J.L. 1967. T h e b o l l w o r m - t o b a c c o b u d w o r m KING, E.G., and MORRISON, R.K. (In Press). S o m e problem in Arkansas and Louisiana. Arkansas Agricultu• systems for production of entomophagous arthropods. In ral Experiment Station Bulletin 720. 66 pp. Advances and challenges in insect rearing, eds. E.G. K i n g and N.C. Leppla. U.S. Department of Agriculture techn i c a l LINGREN, P.D. 1969. Approaches to the management bulletin, Washington, DC, USA. of Heliothis s p p . in c o t t o n w i t h Trichogramma spp. Pages 2 0 7 - 2 1 7 i n Proceedings, Tall Timbers Conference on KNIPLING, E.F. 1979. The basic principles of insect Ecological Animal Control by Habitat Management. 26 - 2 8 population suppression and management. U.S. Depart• Feb 1969, Tallahassee, Fla, USA. ment of Agriculture Agricultural Handbook Washington , D C , U S A 6 5 9 pp. LINGREN, P.D. 1977. Campoletis sonorensis: m a i n t e • n a n c e of a p o p u l a t i o n on t o b a c c o b u d w o r m in a field KNIPLING, E.F., and McGUIRE, J.U., Jr. 1968. P o p u • cage. Environmental Entomology 6: 72-76. lation m o d e l s t o a p p r a i s e t h e limitations a n d potentialities of Trichogramma in managing host insect populations. LINGREN, P.D., and KIM, J.G., 1970. Inundative U.S. Department of Agriculture technical bulletin 138 7 , releases of Trichogramma sp. for control of bollworm and W a s h i n g t o n D C , U S A . 4 4 p p . t o b a c c o b u d w o r m a t t a c k i n g c o t t o n . P r e s e n t e d a t the Annual Meeting of the Entomological Society of Americ a , KOGAN, J., SELL, D.K., STINNER, R.E., BRADLEY, M i a m i , Fla, U S A , 30 N o v - 3 D e c 1 9 7 0 . 6 p. J.R., Jr., and KOGAN, M. 1978. T h e literature o f a r t h r o • pods associated with soybean. V. A bibliography of Helio- LINGREN, P.D., RIDGWAY, R.L., and JONES, S.L. Ihis zea ( B o d d i e ) a n d H.virescens ( F . ) 1 9 6 8 . Consumption by several common arthropod pre• (Lepidoptera:Noctuidae). International Agricultural P u b l i • dators of eggs and larvae of two Heliothis species that cations, University of Illinois INTSOY Series 17, U r b a n a , attack cotton. Annals of the Entomological Society of III, U S A . 2 4 2 pp. A m e r i c a 6 1 : 6 1 3 - 6 1 8 .

KROMBEIN, K.V., HURD, P.D., Jr., SMITH, D.R., and LINGREN, P.D., GUERRA, R.J. NICKELSEN, J.W., BURKS B.D. 1979. C a t a l o g u e o f H y m e n o p t e r a i n A m e r • and WHITE, C. 1970. H o s t s a n d host a g e p r e f e r e n c e o f ica north of Mexico. Washington, DC: Smithsonian Institu• Campoletis perdistinctus. Journal of Economic Entomol• tion P r e s s . 2 7 3 5 p p . ( 3 v o l u m e s . ) ogy 63: 518-522.

LASTER.M.L. 1972. Interspecific hybridization of Helio- LOPEZ, J.D., Jr., RIDGWAY, R.L., and PINNELL, R.E. this virescens a n d H. subflexa. Environmental Entomol- 1 9 7 6 . Comparative efficacy of four insect predators of ogy 1:682-687. the bollworm and tobacco budworm. Environmental Ento• mology 5: 1160-1164. LASTER, M.L. 1974. Increasing natural enemy resour- c e s t h r o u g h c r o p rotation a n d strip c r o p p i n g . P a g e s 1 3 7 - McKINION, J.M., BAKER, D.N., HOSKETH, J.D., and 1 4 9 in Proceedings, Summer Institute on Biological JONES, J.W. 1974. SIMCOTT II, A simulation of cotton Control of Plant Insects and Diseases, eds. F.G. Max w e l l growth and yield, a user's manual. Agricultural Resea r c h

120 Service, U.S. Department of Agriculture, ARS-52, So u t h • populations. Southern Cooperative Series Bulletin 169: e r n R e g i o n . 4 8 - 5 6 .

MORRISON, R.K., JONES, S.L., and LOPEZ, J.D. RIDGWAY, R.L., and VINSON, S.B. (Eds.) 1977. B i o - 1 9 7 8 . A unified s y s t e m for t h e p r o d u c t i o n a n d p r e p a r a • logical control by augmentation of natural enemies. N e w tion of Trichogramma pretiosum for field release. S o u t h • York, USA: Plenum Press. 480 pp. western Entomologist 3: 62-68. RIDGWAY, R.L., and LINGREN, P.D., COWAN, C.B., NEUNZIG, H.H. 1963. W i l d host plants o f the c o r n e a r - Jr., and DAVIS, J.W. 1967. Populations of arthropod w o r m a n d the t o b a c c o b u d w o r m i n e a s t e r n N o r t h C a r o l • predators and Heliothis spp. after applications of sys• ina. Journal of Economic Entomology 56: 135-139. temic insecticides to cotton. Journal of Economic En t o • mology 60: 1012-1016. NEWSOM, L.D. 1975. Pest management: concept to practice. Pages 257-277 in I n s e c t s , s c i e n c e a n d society, RIDGWAY, R.L., KING, E.G., and CARRILLO, J.L. ed. D. Pimentel. New York, USA: Academic Press. 284 pp. 1977. Augmentation of natural enemies for control of plant pests in the western hemisphere. Pages 379-416 in NEWSOM, L.D., and SMITH, C.E. 1949. D e s t r u c t i o n o f Biological control by augmentation of natural enemie s certain insect predators by applications of insectic i d e s to eds. R.L Ridgway and SB. Vinson. New York. USA: Ple• control cotton pests. Journal of Economic Entomology 4 2 : n u m Press. 4 8 0 pp. 9 0 4 - 9 0 8 . RIDGWAY, R.L., ABLES, JR., GOODPASTURE, C, NOBLE, L.W., and GRAHAM, H.M. 1966. B e h a v i o r o f and HARTSTACK, A.W. 1981. Trichogramma a n d its C a m p o l e t i s perdistinctus (Vierick) as a p a r a s i t e of t h e utilization for c r o p protection in t h e U n i t e d States. In P r o • tobacco budworm. Journal of Economic Entomology 59: ceedings, Soviet-American Conference on Use of Bene• 1 1 1 8 - 1 1 2 0 . ficial Organisms in Control of Crop Pests. Entomologi c a l NORDLUND, D.A., JONES, R.L., and LEWIS, W.J. Society of America publication. 62 pp. (eds.) 1 9 8 1 . Semiochemicals: Their role in pest control. ROACH, S.H. 1975. Heliothis spp.: L a r v a e a n d a s s o • New York, USA: John Wiley. 306 pp. c i a t e d p a r a s i t e s a n d d i s e a s e s on wild host plants in t h e OATMAN, E.R., and PLATNER, OR. 1971. Biological Pee Dee area of South Carolina. Environmental Entomol• control of the tomato fruitworm, cabbage looper, and ogy 4: 725-728. hornworms on processing tomatoes in southern Califor• nia, using mass releases of Trichogramma pretiosum. ROBINSON, R.R., YOUNG, J.H., and MORRISON, Journal of Economic Entomology 64: 501-506. R . D . 1972. Strip-cropping effects on abundance of pre• datory and harmful cotton insects in Oklahoma. Environ • PATEL, R.C. 1975. To assess the effectiveness of mass mental Entomology 1: 145-149. releases of laboratory bred Chelonus heliopae G u p t a a n d t o m a i n t a i n c u l t u r e s a n d i m p r o v e b r e e d i n g m e t h o d s o f ROOM, P.M. 1979. Parasites and predators of Heliothis other p a r a s i t e s for u s e in future r e l e a s i n g p r o g r a m s . Final spp. ( L e p i d o p t e r a : N o c t u i d a e ) in c o t t o n in the N a m o i V a l • Technical Report, Project No. A-ENT-90, Gujarat Agr i c u l • ley, New South Wales. Journal of the Australian Entomo • tural University, Gujarat, India. logical Society 18: 223-228.

PINTO, J.D., PLATNER, G.R., and OATMAN, E.R. ROSSLER, Y., BAR, D., GERLING, D., and GON• 1 9 7 8 . Clarification of the identity of several common spe• ZALEZ, D. 1975. Integrated control in cotton: Early sea• cies of North American Trichogramma. Annals of the son pest and natural enemies complexes. I n Entomological Society of America. 71: 169-180. Proceedings. Sixth Scientific Conference of the Israel Entomological Society, Tel-Aviv, Israel. QUAINTANCE, A.L., and BRUES, C.T. 1905. T h e c o t • ton bollworm. U.S. Department of Agriculture Division of SABROSKY, C.W. 1981. A partial revision of the genus Entomology Bulletin 50, Washington DC, USA. 155 pp. Eucelatoria (Diptera, Tachinidae), including important parasites of Heliothis. U.S. Department of Agriculture RABB, R.L., STINNER, R.E., and VAN DEN BOSCH, technical bulletin 1635, Washington DC, USA. 18 pp. R. 1 9 7 6 . Conservation and augmentation of natural ene• mies. Pages 233-254 in Theory and practice of biological SHCHEPETIL'NIKOVA, V.A. 1974. P r i m e n e n i e t r i k h o - control, eds. C.B. Huffaker and P.S. Messenger. New grammy v SSR. Pages 138-158 in Biologicheskie motod- York, USA: Academic Press. ika zashchity rastenii, Kolos, Moscow, USSR.

RAO, V.P. 1974. Biology and breeding techniques for SHEPARD, M., and STERLING, W. 1972. I n c i d e n c e o f parasites and predators of Ostrinia spp. a n d Heliothis spp. parasitism of Heliothis spp. (Lepidoptera: Noctuidae) in CIBC Final Technical Report, U.S. PL-480 Project, Ba n • some cotton fields of Texas. Annals of the Entomologic a l galore, India. 86 pp. Society of America 65: 759-760.

RIDGWAY, R.L., and LINGREN, P.D. 1972. P r e d a c e - SHEPARD, M., LAWN, R.J., and SCHNEIDER, M. (In ous and parasitic arthropods as regulators of Heliothis press). Insects on grain legumes in North Australia: a

121 survey of potential pests and their enemies. Universit y of W H I T C O M B , W . H . 1 9 7 4 . Natural populations of ento- Q u e e n s l a n d P r e s s : B r i s b a n e , A u s t r a l i a . mophagous arthropods and their effect on the agroecosystem. Pages 150-169 i n Proceedings, Summer Institute S H E P A R D , M . , M c W H O R T E R , R.E., a n d K I N G , E.W. o f B i o l o g i c a l C o n t r o l o f Plant I n s e c t s a n d D i s e a s e s , e d s . (In p r e s s ) . B i o l o g y of Pristhesancus papuensis Stal F.G. M a x w e l l a n d F.A. Harris. J a c k s o n , M i s s , USA: U n i v e r • ( H e m i p t e r a : R e d u v i i d a e ) a n d a d e s c r i p t i o n of t h e i m m a • sity P r e s s of M i s s i s s i p p i . 6 4 7 p p . t u r e a n d a d u l t s t a g e s . C a n a d i a n E n t o m o l o g i s t (in p r e s s ) .

W H I T C O M B , W . H . , and B E L L , K . 1 9 6 4 . Predaceous S M I T H , J . W . , K I N G , E.G., and B E L L , J.V. 1 9 7 6 a . Par• i n s e c t s , s p i d e r s , a n d m i t e s o f A r k a n s a s c o t t o n fields. asites and pathogens among Heliothis s p e c i e s i n t h e Arkansas Agricultural Experiment Station bulletin 690, Central Mississippi Delta. Environmental Entomology U n i v e r s i t y o f A r k a n s a s , Fayetteville, Ark, U S A . 8 4 p p . 5 : 2 2 4 - 2 2 6 .

S M I T H , J . W . , S T A D E L B A C H E R , E.A., and G A N T T , W H I T C O M B , W . H . , and E A S O N , R . 1 9 6 7 . Life history C . W . 1 9 7 6 b . A c o m p a r i s o n of t e c h n i q u e s for s a m p l i n g a n d p r e d a t o r y i m p o r t a n c e o f t h e s t r i p e d lynx s p i d e r ( A r a - beneficial arthropod populations associated with cotto n . neida: Oxyopidae). Arkansas Academy of Science Pro• Environmental Entomology 5:435-444. c e e d i n g s 2 1 : 5 4 - 5 8 .

S M I T H , J . W . , a n d S T A D E L B A C H E R , E.A. 1 9 7 8 . P r e • Y O U N G , J . H . , and P R I C E , R . G . 1 9 7 5 . I n c i d e n c e , par• d a t o r y a r t h r o p o d s : s e a s o n a l rise a n d d e c l i n e o f p o p u l a • a s i t i s m , a n d distribution p a t t e r n s of Heliothis zea on t i o n s i n c o t t o n f i e l d s i n t h e M i s s i s s i p p i D e l t a . s o r g h u m , c o t t o n , a n d alfalfa for s o u t h w e s t e r n O k l a h o m a . Environmental Entomology 7:367-371. Environmental Entomology 4: 777-779.

S N O W , J . W . , H A M M , J . J . , and B R A Z Z E L , J.R. Y E N , D . F . 1 9 7 3 . A n a t u r a l e n e m y list of i n s e c t s of T a i - 1 9 6 6 . Geranium carolinianum as an early host for Helio• w a n . T a i p e i , T a i w a n : N a t i o n a l T a i w a n University. 106 pp. this zea a n d H. virescens (Lepidoptera: Noctuidae) in the s o u t h e a s t e r n U n i t e d States, w i t h n o t e s o n a s s o c i a t e d parasites. Annals of the Entomological Society of Amer• i c a 5 9 : 5 0 6 - 5 0 9 .

S T I N N E R , R . E . 1 9 7 7 . Efficacy of inundative releases. Annual Review of Entomology 22:515-531.

S T I N N E R , R.E., R I D G W A Y , R.L., C O P P E D G E , J.R., M O R R I S O N , R.K., and D I C K E R S O N , W . A . 1974. Par- a s i t i s m of Heliothis eggs after field releases of Tricho- gramma pretiosum in cotton. Environmental Entomology 3 : 4 9 2 - 5 0 0 .

S T I N N E R , R.E., B R A D L E Y , J.R., Jr., and V A N D U Y N , J . W . 1 9 8 0 . S a m p l i n g Heliothis spp. o n s o y b e a n . P a g e s 4 0 7 - 4 2 1 in S a m p l i n g m e t h o d s in s o y b e a n e n t o m o l o g y , e d s . M . K o g a n a n d D.C. H e r z o g . N e w York, USA: S p r i n g e r - V e r l a g . 5 8 7 pp.

T O D D , E.L. 1 9 7 8 . A c h e c k l i s t of s p e c i e s of Heliothis Ochsenheimer (Lepidoptera: Noctuidae). Proceedings, E n t o m o l o g i c a l S o c i e t y of W a s h i n g t o n 8 0 : 1 - 1 4 .

V A N D E N B O S C H , R., and H A G E N , K.S. 1 9 6 6 . P r e - daceous and parasitic arthropods in California cotton fields. California Agricultural Experiment Station Bulletin 8 2 0 , U n i v e r s i t y of C a l i f o r n i a , B e r k e l e y , Calif, U S A . 32 p p .

V A N D E N B O S C H , R., L E I G H , T . F . , G O N Z A L E Z , D., a n d S T I N N E R , R . E . 1 9 6 9 . C a g e s t u d i e s o n p r e d a t o r s o f the bollworm in cotton. Journal of Economic Entomology 62:1486-1489

W A N G , F . C . 1 9 7 9 . U s e o f Trichogramma t o c o n t r o l c o t • ton bollworm (Shanshi Province). Shanxi People's Pub• lishing H o u s e . 7 0 p p .

W E N E , G. 1 9 4 3 . Sagaritis provancheri (D.T.), an i m p o r • tant p a r a s i t e o f t h e t o b a c c o b u d w o r m . J o u r n a l o f E c o • nomic Entomology 36:2.

122 The Prospects for the Use of Nuclear Polyhedrosis Virus in Heliothis Management

D.J. McKinley*

Abstract

The choice and development of insect viruses for use in controlling pests is outlined, and the major information sources cited. Although viruses are specific and do not have the harm• ful effects of many chemicals, they are likely to supplement, rather than replace, chemicals. Difficulties in field methodology, lack of information on the crop, pest, and beneficials, and gaps in understanding of viruses are barriers to progress in viral control of insect pests. Viruses isolated from Heliothis include cytoplasmic polyhedrosis viruses (CPVs), granulosis viruses (GVs) and nuclear polyhedrosis viruses (NPVs). Two NPVs have been safety-tested and one-Elcar-is commercially available as a viral pesticide. To develop another virus or to use local production would involve unknown hazards, but the risk could be reduced by simple precautions and quality control. Releasing infected insects or using baits would avoid the real or fancied danger. Some efficacy testing would be required. Full field evaluation and the estimation of "success" present practical difficulties. An assess• ment of published results is given. Although cotton is probably the most difficult crop for virus trials, two successful examples are quoted of virus use for the control of Heliothis armigera. The development of a baculovirus as a pest-management tool appropriate for the local Heliothis armigera requires research; however, there is a sound information base, and the potential tor success appears great.

T h e d e v e l o p m e n t of insect viruses for use in insect o n e s u c h virus, Baculovirus heliothis, t h e singly pest control is clearly illustrated by the history of embedded nuclear polyhedrosis virus (NPV) iso-

*Centre for Overseas Pest Research, London, UK.

International Crops Research Institute tor the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru. A.P., India. 123 lated f r o m Heliothis zea in the USA. The main is given by Burges (1981) in which the chapters on development started in 1961 and reached fruition viruses include the topic of Heliothis virus, virus in 1973, when the Environmental Protection production, and the role of virus in insect pest co n • Agency granted a label for the use of this product trol. This last textbook follows on from Burges and on cotton. Currently it is marketed by Sandoz as Hussey (1971), which contains definitive chapters Elcar in the USA, and there has been some use of on experimental technique. Basic methods have this material in Europe and Australia also. recently been described in compact form, particu• Insect viruses comprising seven major groups larly useful for training, by Kalmakoff and Long- occur naturally and produce diseases in Lepidop- worth (1980). tera, Coleoptera, Diptera, and several smaller The same advantages are stressed in all intro• groups. Viruses have now been isolated and de• ductions to publications on the use of viruses in scribed from some 800 species. Of these known pest control. Viruses are self-replicating and can viruses, many are closely related to others patho• produce epizootics; are naturally occurring and so genic to man, domestic animals, a wide range of nonpolluting; are nonpersistent; may be cheap; and invertebrates, and plants. Only viruses in the Bacu- do not depend for their production on petrochemi• lovirus group have no such dangerous relation• cals. However, real epizootics hardly ever occur ships (Table 1), attacking neither intact organisms outside forests, application in annual crops is sel• nor culture cells or tissues from outside the dom followed by useful persistence to the next Arthropoda, and commonly showing a very narrow season, and intensive safety testing pushes costs host range within the Insecta. By common consent, up. Viruses are slow-acting compared with chemi• research aimed at insect pest control is limited to cals, so that a higher than normal level of crop t h e Baculoviruses (NPVs and granulosis viruses or damage is inevitable. Chemicals used widely are GVs) and to a few of the related cytoplasmic quick-acting and can give excellent control. Some polyhedrosis viruses (CPVs), although these are chemicals are nonpersistent and do little damage treated with caution (Table 2). to some ecosystems, their degradation pathways Research and development of viruses have having been studied, although one suspects that passed through a number of phases: discovery and this is just a matter of relative damage. description, efficacy testing, persistence evalua• Viruses, like all microbials, are potentially very tion, characterization and identification by bio• effective, but they are far more difficult to use than chemical and serological means, genetic analysis, chemicals and must be considered in relation to and investigation of their behavior in the cell. Dur• other components. The use of viruses will never ing the last 8 years, considerable work has been replace other systems, including chemical pesti• carried out on the practical use of these viruses, cides. Nevertheless, the full potential of baculovir• including application technology, safety testing, uses has not been fully exploited yet (Tinsley field testing, and use in pest management. 1979). In particular, the fundamental mechanisms The general status of viruses of invertebrates by which infection takes place and the phenomena was reviewed by David (1975); Falcon (1976) of latency and induction are not understood, and reviewed the problems associated with their com• their elucidation, although the province of the spe• mercialization. Tinsley (1979) has reviewed viruses cialist, may be entirely relevant to the practical in their role as potential pesticides, giving the most application of viruses. Although a number of attrac• concise account available. The technology of virus tive strategies of virus use were suggested by use is a difficult and rather neglected subject, some of the earliest workers in this field and have reliance having inevitably been placed on using the been constantly advocated (Ignoffo 1978), insec- often inappropriate methods used for applying ticidal approaches are still more commonly used, chemicals. Although some of the work has been being relatively straightforward; however, some of d o n e on Bacillus thuringiensis, an attempt has the alternatives such as the release of infected been made to fill this gap, and two symposia were larvae and the dispersal of virus by the adult insect held by the Entomological Society of America, cov• deserve more attention. ering application and formulation (Ignoffo and Fal• The motive behind the decision to use a virus or con 1978) and the related topic of persistence in other microbial has rarely been mere curiosity, and the environment (Hostetter and Ignoffo 1977). A most integrated systems have been developed fol• broader and more complete account of some lowing disasters or potential disasters when chemi• aspects of the whole field of control with microbials cal control fails. Although seldom absolute, the

124 T a b l e 1 . T h e I n s e c t p a t h o g e n i c v i r u s e s .

Biochemical and biophysical N u c l e i c a f f i n i t i e s

G r o u p a c i d Insects affected Vertebrates P l a n t s C o m m e n t s

Nuclear polyhedrosis virus (NPV) and DNA Lepidoptera, N o n e N o n e Moderately fast Granulosis virus (GV) (Baculovirus) Hymenoptera, a c t i n g , D i p t e r a p e r s i s t e n t

Cytoplasmic polyhedrosis virus RNA L e p i d o p t e r a , a R h e o v i r u s P l a n t Highly infective, (Rheoviridae) few Diptera, B l u e T o n g u e rheoviruses slow-acting; Hymenoptera, i n c a t t l e i n f e c t e d l a r v a e C o l e o p t e r a e x c r e t e v i r u s , possibly more genetically labile

Iridovirus (Iridoviridae) DNA D i p t e r a , C o l e o p t e r a , A f r i c a n s w i n e A l g a l Low infectivity Lepidoptera f e v e r , f r o g v i r u s a n d f u n g a l v i r u s e s

Entomopox* (Poxviridae) DNA C o l e o p t e r a , D i p t e r a , B i r d p o x , s m a l l p o x , N o n e P o s s i b l y s t a b l e i n Lepidoptera c o w p o x f i e l d . R e l a t i o n s h i p s w i t h m a m m a l i a n viruses tentative

Densovirus (Parvoviridae) DNA Galleria, Juniona R o d e n t v i r u s e s N o n e (Lepidoptera)

Enterovirus (Picoaviridae) RNA B e e s P o l i o S m a l l R N A Nodamura v i r u s in Gastroenteritis v i r u s e s m o s q u i t o k i l l s t e s t m a m m a l s

Sigma virus (Rhabdoviridae) RNA Drosophila R a b i e s P l a n t r h a b d o v i r u s e s

*Asterisks indicate level of importance as microbial pesticides. T a b l e 2 . V i r u s e s i n l a r g e - s c a l e u s e f o r I n s e c t p e s t c o n tr o l .

P e s t P a t h o g e n C r o p a t t a c k e d C o u n t r y S t a t u s

Agrotis segetum GV C e r e a l s , e t c . P a k i s t a n , D e n m a r k Choristoneura fumiferana NPV T r e e s C a n a d a F u l l y t e s t e d Autograph a californica NPV V e g e t a b l e s , s o y b e a n , USA Registration application s u g a r b e a t , c o t t o n ( o n s o y b e a n , s u g a r b e e t a n d c o t t o n ) Heliothis zea, Heliothis virescens NPV C o t t o n USA Registration EPA 1975 ( E l c a r ) Heliothis armigera. Heliothispunctigera NPV C o t t o n , s o r g h u m A u s t r a l i a Registration Lymantria s p p NPV F o r e s t U S A , D e n m a r k , Registration EPA 1978 S w e d e n ( G y p c h e c k ) Hemerocampa pseudotsugata NPV F o r e s t USA Registration EPA 1976 ( B i o c o n t r o l 1 ) Neodiprin s p p NPV F o r e s t C a n a d a F u l l y t e s t e d , l a r g e s c a l e u s e . Trichoplusia ni NPV C o t t o n C o l o m b i a , L a r g e - s c a l e ( p e s t S . A m e r i c a eradicated) Oryctes s p p CPV C o c o n u t S a m o a L a r g e - s c a l e u s e R h i n o c e r o s b e e t l e CPV C o c o n u t S e y c h e l l e s Large-scale experimental Spodoptera s p p NPV V e g e t a b l e s , c o t t o n e t c . P e o p l e ' s R e p u b l i c L a r g e - s c a l e u s e o f C h i n a Mythimna separata NPV C o t t o n P e o p l e ' s R e p u b l i c L a r g e - s c a l e u s e o f C h i n a Heliothis armigera NPV C o t t o n P e o p l e ' s R e p u b l i c L a r g e - s c a l e u s e o f C h i n a appearance of resistance to chemicals provides effect when fed to 37 other insects, spiders, and the strongest motivation. However the motive is mites, or injected into the hemocoel of four other usually a mixture of scientific and political reasons, insects. There is also confirmation of effectiveness as when a response is made to a strong environ• from field and laboratory studies in Australia, but mentalist pressure group, or is rejected because of some contrary reports from India. Unless it is the presence of a particularly effective insecticide planned to produce a local virus, Elcar would seem industry. Now that there is a general awareness of to be the obvious first choice for any new work, its dangers, pollution is rarely so severe that it since it is a well-formulated and tested product. A cannot be abated by a change of chemical. Deci• laboratory evaluation should however be made sions to turn to microbials rather than to modify the comparing the LD50 of this virus with others using chemical system in pest management will, with the local insects. present state of the art, largely be made as a policy or political decision. My selection of relevant points from the voluminous literature will itself be guide d The Question of Safety by my own preferences and my own experience with Heliothis and Spodopfera littoralis a n d their There are now a great deal of data to support the viruses in Africa, Crete, and Egypt. My aim then is to thesis that the baculovirus group is the safest of all express an opinion, and hopefully to stimulate dis• the known viruses. The definition of safety varies, cussion, rather than to suggest answers. however, with political outlook and social attitude. Burges (1981) describes how microbials, including Heliothis virus, are locally produced and used on Viruses of Heliothis Species communes in China without any local safety test• ing. Although many field trials have been carried T h e g e n u s Heliothis includes a number of impor• out everywhere using crude or purified virus with• tant crop pests; of these, Heliothis zea a n d Heliothis out any safety testing, the USA, UK, and a few virescens in the New World, and Heliothis armigera countries in Europe regulate the use of viruses and in the Old World have been the most closely stud- have laid down protocols for mammalian safety ied. Viruses have been isolated from all the species testing. These protocols are based on the WHO/ that have been sufficiently studied. One Iridovirus FAO (1973) recommendations, and a series of (nonoccluded), at least two cytoplasmic polyhed- guidelines produced by the U.S. Environmental rosis viruses (CPVs), one granulosis virus (GV), Protection Agency (EPA). The evolution of these and two distinct groups of nuclear polyhedrosis protocols is described by Burges (1981). Although viruses (NPVs) have been isolated from the genus. there are differences in that some countries tend to The NPVs have been compared by modern tech• test purified virus and others to batch-test impure niques, including serology and DNA analysis using virus that includes insect cells and many bacteria, restriction endonuclease, and it is clear that there the systems used so far have all been thorough- are structural differences between them. What is some would say too elaborate—and have been less clear is what these structural differences based on safety-testing systems for insecticides mean. Although cross-infectivity has been shown, and pharmaceuticals. They have used small precise comparison of their efficacy, which can mammals and tissue-culture systems and there only be made using the LD50s from individual feed• have been no adverse findings. Since the reports ing bioassays, is not complete. Work is underway, issued are often highly complex documents, the however, in Columbia, Missouri, and at the Glass- Society for Invertebrate Pathology, in an attempt to house Crops Research Institute, UK, where it has clarify the situation, has issued a statement that been found that singly embedded NPVs have very says, "Absolutely no health or environmental similar LD50s and are slightly more effective than hazard has yet been demonstrated which would the multiple-embedded NPV when tested with Heli• prevent the replacement of toxic chemical pesti• othis armigera (Payne and Williams, personal cides by baculoviruses in the control of certain communication). pests" (Kreig et. al. 1980).

Baculovirus heliothis, the NPV in Elcar, is singly Safety testing is expensive, probably unneces• embedded and is known to kill Heliothis armigera, sarily so, but the whole development of Baculovirus paradoxa, phloxiphaga, punctigera, virescens, a n d heliothis is said to have been one-fifth as expensive zea (Burges 1981). It has been found to have no as the development of a conventional insecticide.

127 Safety testing also requires a high degree of organ • from the insect's gut, and inevitably bacteria of ization; where this is lacking, or where a relatively decay, which rapidly multiply in this highly nutri• minor or local pest is the subject, or where the cro p tious insect soup. The decay bacteria in particular attacked is of relatively low value, it is tempting to may be-hazardous. The pathogenicity of unidenti- cut costs and to simplify both production and appli• fied virus, of a mixture of known or unknown viruses cation by using crude methods and omitting safety plus bacteria, cannot be predicted. In fairness, testing and quality control. In almost every case, these bacteria will be no worse than in a natural the early attempts at using viruses, often in quite outbreak, no more hazardous than bacteria in dung large field trials, made use of virus suspensions heaps or open drains. However, one important dif• prepared from insect cadavers and at best crudely ference is that spraying often produces a fine mist filtered. of small droplets; spray operators may be exposed In Zimbabwe, farmers are instructed to control to these for hours at a time. The pathology of the Plusia spp on soybean by spraying with a suspen• inhalation of such mixtures deep into the human sion of diseased larvae stored in the freezer since lung is not known, and neither is the possibility of the last season, or since the last crop cycle. In allergenicity. Although purified viruses are tested Sabah the macerated bodies of the limacodid by inhalation tests and for allergenicity, the con• caterpillars of Dama trima are used to control this tents of crude mixtures are variable and unknown. pest, which attacks oil and coconut palm grown in In developing an insect pathogen, preliminary large plantations. Unskilled labor is used, and it is field testing is usually done on materials that hav e thought that only the simplest testing has been not been safety-tested and that have only been carried out. Examination of samples of the spray crudely purified. The risks are probably no greater have shown the presence of three viruses (Harrap than when performing any operation with crude and Tinsley 1978), a granulosis virus, and two small materials, and I for one have often taken them. The RNA viruses, one of which is like an enterovirus. difficulty is when one expands the experiment into T h e Darna trima control method appears to be a recommendation for control, someone has to very effective and cheap, and there is no evidence issue the details, which will involve suggesting that any of the workers have suffered any harm, exposure of workers to an undefined hazard. In although human blood samples have shown posi• some countries the concern is that the illness of a tive antigen-antibody reactions with one or other of farmer, especially with undefined symptoms, would the two RNA viruses. What are the objections to this be followed by legal action, which in turn might method? The example of Darna trima and the fact cause loss of faith in the insect control method. that virus samples of the NPVs of Trichoplusia ni The decision to make no regulations or recom• (Morris et al. 1978) and Heliothis armigera (Rubin- mendations regarding the safety-testing is logical, stein 1979) have also been found contaminated but is one that might be difficult to justify, although it with small viruses confirm the idea that more than can be explained on the grounds of expediency, or one virus can appear in a batch of insects infected a choice of the lesser of two evils. In circumstanc e s with an NPV. The presence of these viruses is likely where this seems to be the right policy, simple to vary from batch to batch, especially if a sample precautions—especially the wearing of masks and do-it-yourself system is used, if no purification overalls—would reduce the risk, and early steps other than filtration is carried out, even baculovi - should be taken to train the spray operators. Care ruses that are intended to be present will be very should also be taken to select the least hazardous difficult to count, so that the presence of other method of virus application. Sprayers producing viruses, even insect pathogens, will not be detecta• large droplets and thickened spray liquids would ble by bioassay. Although the virus contaminants in reduce what appears to be the worst hazard—the the specific examples quoted have not been generation of aerosol-sized droplets. The use of causes of mammalian disease, small viruses iso• semisolid baits would further protect operators, an d lated f r o m Melolontha were injected into rabbits the release of infected insects would eliminate the and caused a fatal disease. Rickettsia are also inhalation risk altogether. Perhaps the finest actual known to occur in insects, and Rickettsia similar to example of a low-risk situation would be the control those producing fatal fevers in man have been of Oryctes spp in Samoa, where piles of rotting isolated from a Saturniid. sawdust that attract the insects are treated with virus and fungus Metarrhizium anisopliae ( M a r - Finally, spray liquids prepared by crude methods, schall 1980). In Crete I have obtained a high level of especially in a warm climate, will contain bacteria

128 larval kill of Spodoptera littoralis larvae by scatter• stage of widespread use or official recognition ing a porridge-like bait containing NPV on the without serious loss is encouraging. I h a v e dealt g r o u n d under lucerne. with the n e e d to safety-test the actual insect p a t h o • My o w n preference w o u l d be to use a low-risk gen, but o n e constantly v o i c e d c o n c e r n is that a m e t h o d of application a n d a highly purified virus in virus that has been developed, safety-tested, a n d a simple formulation for laboratory investigations used may, through a c h a n c e mutation, c h a n g e into a n d s m a l l - s c a l e field trials, eliminating the worst a h u m a n pathogen. As viruses are self-replicating hazards a n d m a k i n g the determination of virus c o n • they cannot be recalled o n c e released. centration simple, thus giving t h e required d e g r e e Viruses are self-replicating in the insect host, are of precision for both types of study. If this prelimi• variable, and, like all organisms that have the nary a s s e s s m e n t s h o w s efficacy, the next step nucleic-acid-based g e n e system, sho w genetic w o u l d be large-scale field operations, w h i c h w o u l d variation and have the potential for mutation. H o w • follow safety testing. If the virus is p r o d u c e d locally, ever, most insect pathogens have been k n o w n a n d the quality of t h e product should be carefully observed for many years without the a p p e a r a n c e c h e c k e d . of s u c h a hazard. In safety tests, no replication has W h e r e a virus is used in the field, not only the o c c u r r e d in normal intact animals, i m m u n o - target pest but other invertebrates a n d vertebrates suppressed intact animals, or in tissue culture s y s • will be e x p o s e d to the virus as well. Obviously the tems. W h e r e tests have been performed, e.g., kill of other pests w o u l d be an a d v a n t a g e , but what Carey and Harrap (1979), insect viruses have b e e n of the d a n g e r s to beneficials, to f o o d chains, a n d to found not to persist in the vertebrate body. Without the e n v i r o n m e n t generally? Being specific, viruses prolonged exposure to the vertebrate's internal are likely to c a u s e less h a r m t h a n c h e m i c a l pesti• environment, there is no selection a n d so no cides, many of w h i c h are g e n e r a l poisons. This c h a n c e of adaptation to this environment. T h e r e topic w a s reviewed by Bailey (1971). Natural virus are e n o r m o u s numbers of viruses in our habitat that epizootics a n d t h e repeated use of s o m e viruses c a u s e disease in invertebrates a n d vertebrates, have given no indication of d i s e a s e outbreaks in including animals that are our close c o m p a n i o n s . any beneficial. In my o w n field trials in Crete, Spo• Although m a n shares certain diseases p r o d u c e d doptera littoralis larvae f r o m u n s p r a y e d fields w e r e by viruses with domestic a n d wild animals, e.g. collected a n d c o m p a r e d with those c o l l e c t e d f r o m rabies, the a p p e a r a n c e of new virus diseases is fields treated with different levels of virus, by rear• rare. S u c h a possibiity c a n never be eliminated, but ing to death or pupation on artificial diet. Large circumstantial evidence suggests that it is unlikely, n u m b e r s of parasites w e r e obtained f r o m b a t c h e s a n d that the danger should c o m e from a b a c u l o v i • of both uninfected (control) a n d lightly infected lar• rus s e e m s very improbable. M o d e r n research on vae. Burge s (1981) reports that extensive patho• viral genetics—not on genetic engineering, w h i c h logical examinations on h o n e y b e e s s h o w e d no has received official discouragement, but in the sign of any virus disease. In general, further investi• selection of lines from single n u c l e o c a p s i d s , gations w o u l d be required w h e n a virus is intro• c o u p l e d with testing in m a m m a l s — s h o u l d reveal d u c e d to n e w areas but c a n be c o n f i n e d to types of any s u c h hazard, if it exists, more quickly t h a n it beneficial o r g a n i s m s that are not present in the would appear in the control situation. native habitat of the virus. Baculovirus heliothis Another, more tangible, c a u s e for c o n c e r n is that (Elcar), being registered by the EPA, has bee n most the selection of viral a n d insect strains will lead to completel y tested, while a similar NPV, isolated the a p p e a r a n c e of insect resistance as it has d o n e from Heliothis armigera, has been safety-tested in so often with c h e m i c a l pesticides. It is quite easy to the UK. c o m p o s e a strong argument for or against this possibility. In the laboratory, however, populations of Heliothis zea have been subjected to heavy Are Viruses too Great a Risk? selection pressure using Baculovirus heliothis for 20 to 25 generations without the a p p e a r a n c e of T h e u s e of virus inevitably involves risk—the risk resistance (Ignoffo and Allen 1972) a n d similar that s o m e o n e involved in the p r o g r a m will b e c o m e results were obtained with Heliothis armigera ill, t h o u g h not necessarily from the virus, a n d the (Whitlock 1977). It has bee n reported that different risk of losing m o n e y . A list of the major s u c c e s s f u l strains of Baculovirus heliothis exist with a 56-fold viruses ( T a b l e 2) that have b e e n d e v e l o p e d to the range of activity towards the insect. In Spodoptera

1 2 9 frugiperda, Reichelderfer and Benton (1974) dem• virus to be produced by government agencies, as onstrated the existence of strains with a fivefold in Canada (sawfly viruses by the Canadian For• difference in activity. The existence of virus strains estry Service) and the USA (Douglas fir tussock, differing in their protein structure has also been moth NPV by the USDA), or by groups of farmers, demonstrated in Spodoptera littoralis (Merdan et al. as in the communes of the People's Republic of 1977). In our work on the susceptibility of wild po p • C h i n a . ulations, preliminary work has shown only an approximate fivefold difference that would be accounted for by the natural vigor of wild insects. Efficacy Testing Selection of a codling moth virus for resistance to ultraviolet light was achieved after only four pas• The establishment of LD50s using a healthy insect sages (Brazzel and Benz 1979). colony is an essential part of any control program Although it is difficult to generalize, it would se e m with viruses. It is only the LD50, involving the dosing that some viruses are relatively easily selected for of individual insects, that can give an absolute certain characters, but that selection for resistance means of checking the virus for activity, and the usually fails. Part of the difficulty here is that the target population for changes in susceptibility. With infection mechanisms, the disease process, and t h e Heliothis viruses, testing techniques have been the cause of differences in susceptibility between worked out in detail, and if known viruses are used, insects are not understood, and this lack of knowl• these need to be checked against the published edge is a serious barrierto progress (Tinsley 1980). value. Once this has been done, only periodic Until this barrier is overcome or until a well- checks are needed, using an established test authenticated case of appearance of a resistant colony. strain of insect is described, the risk remains Mass-dosing (LC50) bioassays, which are eas• hypothetical. ier to perform, should be used to determine the Another risk is that of financial loss. Develop• persistence of virus deposits on artificial and nat u • ment of a control system is greatly aided if the virus ral targets under local conditions. A comparative is produced in a standard formulation, and this is a technique, making use of standard suspensions, is field in which commercial organizations have most appropriate. The exposure of virus samples to the of the expertise. Virus development is usually environmental conditions in a particular place or on regarded as being commercially unattractive, a particular crop should be reinforced by physical because the virus itself cannot be patented at the measurements of ultraviolet light, temperature, moment, and many viruses have a narrow host etc., but these measurements are secondary, and spectrum, which limits the potential market (Surges simple instruments will suffice. 1981; Falcon 1976). At present, viruses must be Viruses used in control should be characterized produced in live insects, which is expensive, so that precise identification is possible. Several although production costs have been cut in the kinds of Heliothis virus have already been charac• USA for some insects through automation of the terized, and the task is easy if done by specialists. rearing process. Production in tissue culture sys• Identification does not have to be repeated often, tems is the subject of intensive research in the US A so that the relatively specialist techniques involved and Europe, and a breakthrough in this technology are not a serious disadvantage. The relatively new could significantly reduce costs of production and serological technique, ELISA (enzyme-linked purification. However unattractive virus production immunosorbent assay) (Kelly et. al. 1978; Crook appears, the first registered viral pesticide, Elcar, and Payne 1980), is being developed for the was produced by a commercial company, Sandoz assessment of virus samples, e.g. in infected lar• (Elcar currently costs $ 7.8/ha treatment), and vae, or on sprayed leaves, and requires little exper• there has been some interest shown in the devel• tise, is very quick and simple, and should be widely opment of broad-spectrum viruses such as Auto- u s e d . grapha californica, which may soon be registered. There has also been commercial interest in the production of novel formulations. Generally, a Is Heliothis Virus Successful? period of world trade recession is not a time to expect commercial innovation. The alternative, The heading is deliberately vague. Exact definition which may be suitable in some countries, is for the of success is difficult, and aims should be clearly

130 u n d e r s t o o d as a guide to research. In general, In Australia, s u c c e s s e s w e r e obtained using d a m a g e thresholds should be established, a n d Heliothis NPV on cotton, following a laboratory- a c c e p t a b l e levels a g r e e d upon in a d v a n c e . Viruses screening program; yield increases w e r e obtained hardly ever give the s a m e quickly established c o n • although it was necessary to a c c e p t a m o d e r a t e trol a n d u n d a m a g e d c r o p s that c h e m i c a l insecti• standard of control a n d the a s s o c i a t e d level of c i d e s c a n . In the last t w o d e c a d e s b e t w e e n 150 d a m a g e . a n d 2 0 0 field tests w e r e carried out using Baculovi- Cotton is generally a c c e p t e d as being a difficult rus heliothis, 6 0 % on cotton, 3 0 % on maize, a n d the c r o p on w h i c h to test the control of individual pest rest on s o y b e a n , s o r g h u m , t o b a c c o , a n d tomato. species a n d on w h i c h to use viruses. T h e plants T h e tabulation of these results given by Burges c o m p e n s a t e for early damage, a n d virus inactiva- (1981) is c o n d e n s e d in T a b l e s 3, 4, a n d 5. It is clear tion on the cotton leaf is particularly rapid d u e to the from t h e s e that results are often not equal to those interaction of ultraviolet light, high temperature, a n d obtained with c h e m i c a l s . In the U S A in 1978, e n t o • the moderate to high alkaline conditions that s o m e • mologists using this virus h a d mixed opinions about times o c c u r (Yearian a n d Y o u n g 1974). A b u d a n d it, the verdict of s o m e being that Heliothis popula• boll feeder like Heliothis is difficult to kill with any tions on s o m e of the cotton trials w e r e not sufficient pesticide acting through the gut, a n d an unusually to c a u s e significant c r o p loss, a n d a g r o n o m i c f a c • efficient spray cover is necessary. Considerable tors a n d the p r e s e n c e of other pests w e r e m o r e important. However, e v e n on c o t t o n , w h i c h is a difficult crop, s o m e s u c c e s s e s are clear. It is also Table 4. Yield ratiosa from cotton and maize trials evident that c r o p selection is important, a n d s u c • with virus and Insecticide treatment for H e l i o t h i s c e s s e s on cotton w e r e less evident t h a n on maize; c o n t r o l . control on s o r g h u m w a s frequently better, a n d c o n • trol on s o y b e a n best of all. C r o p a n d I n f e s t a t i o n l e v e l My o w n e x p e r i e n c e of using Heliothis virus t r e a t m e n t L i g h t M e d i u m H e a v y against H. armigera w a s that although g o o d per• sistence on cotton w a s easily d e m o n s t r a t e d with C o t t o n leaf bioassays a n d test insects, larval kill under A 1 . 1 1 1 . 4 8 2 . 2 2 very heavy attack c o u l d not be d e m o n s t r a t e d . B 0 . 9 7 1 . 0 1 0 . 9 7 Using NPV to control Spodoptera littoralis in Egypt, M a i z e we have d e m o n s t r a t e d c r o p protection in t e r m s of A 1 8 . 1 2 2 . 6 3 1 . 0 8 leaf d a m a g e , but in two s e a s o n s of low populations B 0 . 6 2 0 . 7 8 1 . 5 6 w e h a v e f o u n d n o d e m o n s t r a b l e c r o p loss e v e n o n untreated controls. H o w e v e r , trials in the Republic of South Africa against H. armigera on cotton w e r e Source: Burges (1981). very e n c o u r a g i n g , s h o w i n g yield increases c o m • a . A = v i r u s t r e a t e d : c o n t r o l ; parable to those obtained with c h e m i c a l s . B = v i r u s t r e a t e d : i n s e c t i c i d e t r e a t e d .

Table 3. Mean cotton yield ratios (treated: control) f o r 3 8 field trials o f B a c u l o v i r u s h e l i o t h i s on cotton, Table 5. Effect of application of Baculovirus heliothis 1 9 6 3 - 6 7 . on Heliothis populations and damage on soybeans.

L i g h t t o V i r u s m o d e r a t e application R e d u c t i o n R e d u c t i o n H e a v y H. zea D o s e Heliothis zea r a t e i n l a r v a l i n p o d infestations ( P I B / 0 . 4 h a ) infestations ( P I B / 0 . 4 h a ) p o p u l a t i o n (%) d a m a g e (%)

6 x 1 01 0 1 . 0 6 1 . 0 7 9 6 0 x 1 0 1 0 1 . 2 4 2 . 1 7 6 x 10 9 2 7 5 9 6 0 0 x 1 01 0 1 . 3 4 2 . 2 6 6 0 0 x 10 1 0 0 9 0

Source: Burges (1981) Source: Burges (1981).

1 3 1 effort is being put into developing more efficient extended to include the effect of mixed applica• application techniques. In our cotton trials in Egypt tions. In spite of many reports of synergistic effects we have obtained much improved spray cover by from laboratory testing, none of these has been developing our own spray lance and by adopting a definitely proved in the field. Even a simple additive fan-assisted ultralow-volume sprayer. Almost all effect may be worth applying, however, and the trials in which ultraviolet protectants have been combination of NPV, Bacillus thuringiensis, a n d tested have shown marked improvements, but chemicals in a simple routine seems to be a useful even greater benefits have been obtained through approach, exploiting the particular properties of the addition of feeding stimulants such as Coax each material. and molasses. Chemical control of Heliothis is producing Successes with NPV applied to sorghum are clearly recognizable problems in many countries. related to the localized feeding of the larvae in the In the Namoi Valley of Australia, problems have heads, which are easily covered with spray or dust, arisen with multiple resistance to chemicals and and to the absence of growth dilution. Even greater the destruction of an extensive predator fauna; in successes were obtained with NPV on soybean. many southern states of the USA, pesticide used Again, the advantage arises from the feeding mainly to control boll weevil has resulted in severe behavior of the Heliothis larvae on these plants, Heliothis control problems; and in South Africa and possibly from the denser canopy and the chemical Zimbabwe, serious outbreaks of cotton red spider conditions on the leaves. Kill on tobacco was very mite result from the slightest mistake in the routine. high, but the inevitably slow action of the NPV Where problems are acute, or where the crop resulted in unacceptable damage levels. attacked by Heliothis is of real importance, positive The overall picture of the success of Baculovirus action is required. heliothis is encouraging. There seems no doubt Ringing the changes with chemical pesticides is that the virus can give a high level of kill and so m e • probably effective only in the short to medium term. times effective control. The variable success on One of the effects of the world economic recession different crops or on the same crop in different has been a reduction in the rate at which new areas or at different times, underlines a basic chemicals are being produced by industry. Where weakness. This weakness, recognized by most resistance is appearing, there is really no alterna• practical entomologists, is that in spite of a great tive to a policy of developing chemical use, classi• deal of research effort, our understanding of the cal biological control, cultural control, and complex ecology of field-crop pests is very limited. microbial pesticides, including viruses, to produce This limitation is particularly apparent when we are an integrated system before it is too late. The sys• trying to use a highly specific control agent such as tem developed may be relatively cheap and simple, NPV. Studies of the interrelationships between pest or relatively expensive, particularly in terms of and virus have been neglected; where they have trained manpower in the beginning, but in many been undertaken, the results have been rewarding areas, the long-term alternative is disaster. (Entwistle and Adams 1977), and lack of this infor• Local and national politics may make such an mation is the second great barrier to progress. On integrated system unattainable, but there seems some crops, especially where they are attacked by little justification for scientists not to try and initiate a number of different pests, the results of using NPV cooperation between institutions, states, or coun• in the same manner as an insecticide are difficult to tries that have a common Heliothis problem, so that assess. Where it is possible to choose, it would be the cost of developing the individual components of best to carry out the first field tests using this such a system can be divided. It is now generally approach on the most favorable crop, e.g., soybean accepted that Baculovirus heliothis, other NPVs, or Dolichos bean, and to determine the effect of and other microbials have great potential, provided spraying on immediate kill, crop protection, and they are used as components of IPM systems. possibly on long-term population reduction.

In many countries it seems that insecticidal control of Heliothis still works well; here, the advantage Use of Heliothis NPV in Pest- of using NPV would be to reduce chemical applica- Management Systems tions and perhaps ward off the appearance of resistance to chemicals. It is mainly in such situations Baculovirus heliothis has been repeatedly field- that a simple approach is adopted, often being tested on different crops in the USA in areas where

132 Heliothis is a problem. In the Mississippi Delta area, is particularly destructive, where there is a serious cotton is attacked by both the boll weevil and Helio• problem of insecticide resistance, and where it is this zea and chemicals applied to control these desirable to benefit from an extensive fauna of pests results in the destruction of predators, result• beneficials (Room 1979). The sampling data col- ing in heavy crop loss. The control of overwintering lected daily include records of Heliothis larval weevils was the first step; this was followed by the numbers in six age categories, records of 32 other replacement of some early sprays against Heliothis arthropods, including pests, meteorological data, by sprays of virus, giving reasonable control of this and plant-growth data. Predictions of pest popula- pest and eliminating destruction of beneficials. tions were found to be correct on 93 out of 109 Virus application rates as low as 20 larval equiva• occasions, although they could only be made a few lents/acre on 20- to 30-acre plots gave final yields days ahead. better than or equal to chemical application alone In order to maximize the effect of beneficials on (Allen et al. 1966). Similar results were obtained in Heliothis populations, Elcar was used to replace Arkansas, where NPV was used for early-season chemicals below a defined level. In the 2 test years, Heliothis control in a generally simpler pest situa• NPV was applied five times, with five applications of tion. In the latest review in Burges (1981), these chemicals on managed fields, as compared with 16 trials are mentioned, but there is no record of the applications of chemicals on commercial fields. establishment of an IPM system on farms in these Although Heliothis kill and the reduction of damage areas. Publications show that work on the compo• was only moderate on managed fields, the yields nents of these systems continues, but it may be that were slightly superior, and given realistic costing resistance by the farming community, mentioned to (bearing in mind that reduced costs will almost me in 1978, has meant that farmers prefer to con• certainly result from improved methods of virus tinue to rely on chemical programs. In Texas, there production in the future), costs should be lower was a serious problem of resistance of Heliothis to than with commercial practice. There is consider• chemicals, but this has apparently been mitigated able reluctance by farmers to adopt the pest- by more controlled use of the synthetic pyrethroids, management technique, as they find it hard to a massive release of Trichogramma, and some use relinquish the quick, clean results of chemicals an d of NPV sprays. to accept what appear to be high larval populations In the soybean-growing areas, e.g., Missouri and and damage levels. Florida, there has been an intensive effort to develop an IPM system using a computer program Conclusions to predict populations and to make decisions. The crop is attacked by a number of pests, several of There are a number of Baculovirus isolates availa• which are susceptible to pathogens, including ble for the control of Heliothis spp. Two of these Baculovirus heliothis and the fungus Nomuraea have been safety-tested, one of which was isolated rileyi. Soybean was judged to be particularly suit• from Heliothis armigera (Kelley et al. 1980), and the able for the use of virus, and to be amenable to other, more fully developed in the USA, is in com• changes in agronomic practice. Conservation of mercial production by Sandoz and marketed at a the extensive fauna of beneficial arthropods, the present price of U.S. $ 40/kg and an estimated cost use of chemicals, spraying with Elcar, and the of $ 7.8/ha treatment. Results from field trials are application of Nomuraea, coupled with changes in somewhat mixed, depending on the crop treated crop spacing, are all parts of this system. Recent and the other pests present. Further research is papers indicate that particular emphasis is now needed both on the fundamental mechanisms being placed on the Nomuraea component. There involved in the disease process and in the epidemi• are no reports of expansion into commercial areas, ology. NPV has usually been employed in the same perhaps because Elcar is not yet registered for use manner as chemicals but is usually less quick- in crops other than cotton. acting and less efficient. Since it is highly specific, it Finally, there are reports from Australia of gen• avoids resistance problems and the destruction of eral successes with Baculovirus heliothis, follow• beneficials, and since it is not a general poison, ing screening of a number of NPVs. A complex IPM avoids harmful effects in food chains. Full assess• system using a computer has been developed and ment of the long-term benefits has not been made. run for 2 years for the control of cotton pests in the Selection of the right crop, preferably one with few Namoi Valley of New South Wales, where Heliothis pests other than Heliothis, is important.

133 C o s t s are e s t i m a t e d to be lower t h a n wit h Bacil• BURGES, H.D. 1981. Microbial control of pests and lus thuringiensis, but a r e relatively high in propor• plant diseases, 1970-1980. New York: Academic Press. tion to t h e kill obtained, although e x p e r i e n c e in BURGES, H.D., and HUSSEY, N.W. (eds.) Australia suggests that with chemicals control may 1 9 7 1 . Microbial control of insects and mites. New York: be unnecessarily complete. Production costs are Academic Press. high, b e c a u s e t h e virus is p r o d u c e d in live insects, CAREY, D. and HARRAP, K.A. 1979. Safety tests on while stringent safety-testing r e q u i r e m e n t s a d d to the NPVs of Spodoptera littoralis a n d S. exempta. In Inver- t h e costs. It is likely that p r o v e d p r o d u c t i o n t e c h • tebrate tissue culture, developments and applicatio n s niques, especially in cell cultures, will eventually (eds. E. Rurstak and K. Maramorosch). New York: Aca- r e d u c e c o s t s , a n d safety-testing requirements demic Press. h a v e already b e e n modified. CROOK, N.C., and PAYNE, C.C. 1980. Comparisons of U s e of unpurified a n d untested virus in c r o p s three methods of Elisa for Baculoviruses. Journal of Gen• involves hazards that c a n n o t be quantified, but in eral Virology 46: 29-37. some circumstances techniques such as the DAVID, W.A.L. 1975. The status of viruses pathogenic release of infected larvae w o u l d r e d u c e t h e s e for insects and mites. Annual Review of Entomology 2 0 : hazards to those encountered in natural epizootics. 9 7 - 1 1 9 . T h e insecticide m e t h o d (inundative release) of virus use is not likely to r e p l a c e c h e m i c a l s , but ENTWISTLE, P., and ADAMS, D. 1977. Prolonged ret• u s e d against low Heliothis populations should often ention of activity in the NPV of Gilpina hercyniae on allow chemical applications to be reduced. Popula• foliage of spruce species. Journal of Invertebrate P a t h o l • ogy 29: 392-394. tion reduction in multicrop a r e a s a n d t h e d e v e l o p • ment of integrated pest-control systems will FALCON, LA. 1976. Problems associated with the use depend on local conditions, but may initially involve of arthropod viruses in pest control. Annual Review of complicated systems costly in terms of scientific Entomology 21: 305-333. m a n p o w e r . In areas w h e r e the d e v e l o p m e n t of res• FAO/WHO (Food and Agriculture Organization/ istance to c h e m i c a l s is a p r o b l e m , the use of IPM World Health Organization). 1973. Report of the Joint seems almost inevitable. FAO/WHO Meeting on Insect Viruses, Nov 1972, Gen•

Successful systems require not only scientific eva, Switzerland. WHO publication VIR/VBC/73.1.35 pp.

input but a f a r m i n g c o m m u n i t y p r e p a r e d to a c c e p t HARRAP, K.A., and TINSLEY, T.W. 1978. The interna• innovation a n d a c r o p p i n g s y s t e m that c a n be tional scope of invertebrate virus research in cont r o l l i n g manipulated. U n d e r s t a n d i n g of: (1) the beneficials p e s t s . In Viral pesticides: present knowledge and poten• c o m p l e x , (2) the relationship b e t w e e n pest d a m a g e tial effects on public environmental health, (eds. M.D. a n d yield, a n d (3) the e c o n o m i c s of local a g r i c u l • Summers and C.Y. Kawanishi). Environmental Protecti o n Agency-600/9-78-026, Washington, DC, USA. ture, is essential. A p h a s e d r e s e a r c h p r o g r a m on

the use of virus of Heliothis s h o u l d be p l a n n e d to HOSTETTER, P.L., and IGNOFFO, C.M. 1977. Envir• m a k e full use of t h e c o n s i d e r a b l e b o d y of i n f o r m a • onmental stability of microbial insecticides. Entom o l o g i • tion available. cal Society of America miscellaneous publication 10(3): 1-128.

References IGNOFFO, C.M. 1978. Strategies to increase the use of entomopathogens. Journal of Invertebrate Pathology 3 1 ( 1 ) : 1 - 3 . ALLEN, G.E., GREGORY, B.G., and BRA2ZEL, J.R. 1 9 6 6 . Integration of the Heliothis nuclear polyhedrosis IGNOFFO, C.M. 1979. The first viral pesticide: past, virus into a biological control programme on cotton . J o u r • present and future. Pages 105-115 in Development of nal of Economic Entomology 59: 1333-1336. industrial microbiology. Monticello: Lubrecht and C r a m e r .

BAILEY, L. 1971. The safety of pest insect pathogens for IGNOFFO, C.M., and ALLEN, G.E. 1972. Selection for beneficial insects. Pages 491 -505 in Microbial control of resistance to a NPV in laboratory populations of th e c o t t o n insects and mites (eds. H.D. Burges and N.W. Hussey ). b o l l w o r m Heliothis zea. Journal of Invertebrate Pathology New York: Academic Press. 20:187-192.

BRAZZEL, J.R., and BENZ, G. 1979. Selection of a IGNOFFO, C., and FALCON, K.A. 1978. Formulation strain of the granulosis virus of the Codling Moth w i t h and application of microbial insecticides. Entomolo g i c a l improved resistance against artificial u-v radiatio n a n d Society of America miscellaneous publication 10(5): 1 - sunlight. Journal of Invertebrate Pathology. 33:358 - 3 6 3 . 6 8 .

1 3 4 K A L M A K O F F , J . , a n d L O N G W O R T H , J . F . 1980. A c h i e v e m e n t s , D e f i c i e n c i e s , a n d I n n o v a t i o n s . B o y c e Microbial control of insect pests. New Zealand Depart• T h o m p s o n Institute, C o r n e l l University, I t h a c a , N Y , U S A . m e n t o f Scientific a n d Industrial R e s e a r c h Bulletin 2 2 8 W H I T L O C K , V . H . 1 9 7 7 . Effect o f larval m a t u r a t i o n o n Wellington, New Zealand. mortality induced by nuclear polyhedrosis and granulo s i s K E L L Y , D . C . , E D W A R D S , M.L., and R O B E R T S O N , virus infections of Heliothis armigera. J o u r n a l of I n v e r t e • J . S . 1 9 7 8 . T h e u s e o f e n z y m e l i n k e d i m m u n o s o r b e n t brate Pathology 30:80-86. a s s a y to d e t e c t a N P V in Heliothis armigera larvae. J o u r • Y E A R I A N , W . C . , and Y O U N G , S.Y. 1 9 7 4 . Persistence nal of General Virology 40: 465-469. of Heliothis NPV on c o t t o n plant parts. E n v i r o n m e n t a l K E L L Y , D . C . , B R O W N , D.A., R O B E R T S O N , J . S . , and Entomology 3(6):1035-1036. H A R R A P . K.A. 1 9 8 0 . Biochemical, biophysical and sero• l o g i c a l p r o p e r t i e s o f t w o single e n v e l o p e d n u c l e a r polyhedrosis viruses from Heliothis armigera a n d Helio• this zea. 3: 3 1 9 - 3 3 1 .

K R E I G , A . , F R A N Z , J . M . , G R O N E R , A . , H U B E R , J . , and M I L T E N B U R G E R , H . 1 9 8 0 . Safety of entomopathogenic viruses for control of insect pests. Environment a l Conservation 7(2):158-160.

M A R S C H A L L , K.J. 1 9 8 0 . Progress in microbial control: c o c o n u t s . P a g e 31 in Proceedings, W o r k s h o p on I n s e c t Pest M a n a g e m e n t with Microbial Agents: R e c e n t A c h i e v e • ments, Deficiencies, and Innovations Boyce Thompson Institute, C o r n e l l University, Ithaca, N Y , U S A .

M E R D A N , A., C R O Z I E R , L., V E Y R U N E S , J - C . , a n d C R O Z I E R , G . 1977. Etude comparee des proteines des polyedres et des virions de trois isolats de baculovir u s d e Spodoptera littoralis. E n t o m o p h a g a 2 2 ( 4 ) : 4 1 3 - 4 2 0 .

M O R R I S , T . J . , H E S S , R., P I N N O C K , D . , and S C H L E G E L , D . E . 1 9 7 8 . Isolation of a n o n - o c c l u d e d virus associated with baculovirus infections in Trichoplu- sia ni. P a g e 5 6 4 in A b s t r a c t s of t h e F o u r t h International C o n g r e s s for Virology, 3 0 A u g - 6 S e p t 1 9 7 8 , T h e H a g u e , Netherlands.

PESTICIDES SAFETY PRECAUTIONS SCHEME. 1 9 7 9 . Registration criteria for biological agents used as pesticides. London, UK: Ministry of Agriculture, Fisheries a n d F o o d .

R E I C H E L D E R F E R , C . F . , a n d B E N T O N , C . V . 1974. S o m e g e n e t i c a s p e c t s of t h e r e s i s t a n c e of Spodoptera frugiperda to a nuclear polyhedrosis virus. Journal of Invertebrate Pathology 23:378-382.

R O O M , P . M . 1 9 7 9 . A p r o t o t y p e ' o n - l i n e ' s y s t e m for m a n • a g e m e n t o f c o t t o n p e s t s i n t h e N a m o i Valley, N e w S o u t h Wales. Protection Ecology 1:245-264.

R U B I N S T E I N , R. 1 9 7 9 . A n o n o c c l u d e d virus of t h e A m e r i c a n B o l l w o r m Heliothis armigera. Phytophylactica 11:179-180.

T I N S L E Y , T . W . 1 9 7 9 . T h e potential o f i n s e c t p a t h o g e n i c viruses as pesticidal agents. Annual Review of Entomo l • o g y 2 4 : 6 3 - 8 7 .

T I N S L E Y , T . W . 1 9 8 0 . Progress in microbial control: p a t h o g e n s . A.Virus. In P r o c e e d i n g s , W o r k s h o p on I n s e c t Pest M a n a g e m e n t w i t h M i c r o b i a l A g e n t s : R e c e n t

135

The Potential Use of Microbials in Heliothis Management

Marion R. Bell*

Abstract

Studies have shown that all of the major groups of entomopathogens contain organisms with some potential for use in Heliothis management. The use of these microbials may vary con• siderably between crops and locations, depending upon climate, disease symptomatology, and economic thresholds of crop damage. In general, the microbials function naturally in the environment as population suppressors, and as such, ideally function as elements in integra• ted pest management (IPM) programs. The manipulation of pathogens in such management programs offers the greatest potential for their use at this time. The majority of the research on microbial control of Heliothis has been conducted in cotton using the bacterium, Bacillus thuringiensis Berliner, and nuclear polyhedrosis viruses. These pathogens are presently used to suppress low to moderate populations of larvae in cotton within the IPM framework. Recent studies have indicated that using gustatory-stimulant adjuvants can increase the effectiveness of the microbials, and can result in the control of higher populations of Helio• this than nonvally feasible. However, the current use of such induced epizootics as single- factor methods tor control is negligible, compared with the less costly chemical control meth• ods. Although the immediate future tor sizable markets of microbials apparently lies within the IPM programs, the potential for use in unresearched areas remains high.

Insect pathogens, or microbials, act naturally to time, observed extensive epizootics, usually by the limit populations of crop pests, as do other natural occluded viruses, in insect populations. Such an control factors. Most people who have been epizootic might have completely destroyed a popu• involved in agricultural field studies have, at some lation of lepidopteran larvae; however, the crop is often seriously damaged before the population is

*U.S, Department of Agriculture, Agricultural Research Service. destroyed. These observations have spurred Western Cotton Research Laboratory, Phoenix, Ariz. USA. research into microbial control of insects.

International Crops Research Institute tor the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. 137 Theoretically, the p a t h o g e n s m a y be useful in h a v e disadvantages: they are often rapidly d e a c t i • several w a y s . Most of t h e r e s e a r c h , a n d t h e appar• vated by environmental factors, they must be pro• ent potential for microbials in Heliothis m a n a g e • d u c e d in living hosts, a n d they must be ingested by ment, involves the application of p a t h o g e n the host prior to infection. Further, the time from formulations in a m a n n e r similar to that of c h e m i c a l ingestion of a lethal d o s e until d e a t h under field insecticides. However, another m e t h o d is the use conditions may range f r o m 3 to 15 days; during this of inoculative applications of microbials that result time, feeding generally c o n t i n u e s up until the last 2 in s u b s e q u e n t colonization of the p a t h o g e n in the days. Plainly, the incubation period of n u c l e o p o - pest population. This m e t h o d apparently fares best lyhedrosis should be recognized a n d c o n s i d e r e d in in situations w h e r e m o d e r a t e populations or d a m • a m a n a g e m e n t program. a g e c a n b e tolerated. Microbials have m a n y characteristics ideally suited for use in p e s t - m a n a g e m e n t programs. T h e y Bacteria: Bacillus thuringiensis Berliner are usually specific a n d highly virulent on given hosts, p o s e little hazard to nontarget organisms, By far the most promising b a c t e r i u m available for a n d are usually c o m p a t i b l e with other m a n a g e m e n t microbial control of insects is Bacillus thuringiensis programs. A l t h o u g h s o m e d e g r e e o f s u c c e s s has Berliner (B.t.). This b a c t e r i u m is already widely b e e n a c h i e v e d with their use in the m a n a g e m e n t of used against harmful Lepidoptera in several c o u n • Heliothis, they are at present used very little c o m • tries. Like the NPV viruses B. thuringiensis must be p a r e d with c h e m i c a l pesticides. This is d u e not so ingested by larvae before it c a n have any effect. m u c h to the lack of the p a t h o g e n s ' potential as to However, the bacillus has a wider host range, it c a n the user's lack of understanding of the nature of the be p r o d u c e d using fermentation t e c h n i q u e s , a n d it pathogens. Furthermore, m e t h o d s for effective use is not as easily destroyed by the e n v i r o n m e n t as a have not yet been d e v e l o p e d in m a n y areas. virus is. Further, since m u c h of its effect is d u e to the action of a toxic, proteinaceous crystal, the incubation period is shorter a n d the effect m o r e Available Entomopathogens rapid, resulting in less plant d a m a g e . S i n c e it does have a relatively w i d e host range, B. thuringiensis W h a t c a n we expect from microbial control? In must be used with s o m e c a r e to k e e p it out of order to u n d e r s t a n d the potential of various p a t h o • lepidopteran insect-rearing facilities. g e n s in Heliothis m a n a g e m e n t , we must c o n s i d e r their individual pathological characteristics. Stu• dies h a v e s h o w n that most of the major g r o u p s of Fungi: Fungi Imperfecti e n t o m o p a t h o g e n s contain o r g a n i s m s with s o m e potential for use in Heliothis m a n a g e m e n t . Their T h e fungi imperfecti c o m p r i s e m a n y s p e c i e s in a use m a y vary considerably b e t w e e n c r o p s a n d variety of g e n e r a that are infectious to insects. locations, d e p e n d i n g upon climate, d i s e a s e s y m p • A m o n g these are several species that have been tomatology, a n d e c o n o m i c thresholds of c r o p d a m • c o n s i d e r e d a n d tested for Heliothis management, age. T h e following are brief descriptions of the including Beauveria bassiana (Bals.) Vuillemin, characteristics of representative microbials a n d Metarrhizium anisopliae (Metsch.) Sorokin, a n d s u b s e q u e n t diseases that have b e e n studied for Nomuraea rileyi (Farlow) S a m s o n , formerly k n o w n use in Heliothis management. as Spicaria rileyi. T h e s e fungi are c o m m o n l y o b s e r v e d as the c a u s a t i v e agents of natural e p i • zootics a n d have a relatively w i d e host range. T h e y Viruses: Nuclear Polyhedrosis differ f r o m the viruses, bacteria, a n d protozoa that Viruses (NPVs) h a v e bee n c o n s i d e r e d for control of Heliothis in that ingestion is not usually required for infection, as T h e NPVs are c o n s i d e r e d to have g o o d potential in these o r g a n i s m s c a n penetrate through the sur• i n s e c t - m a n a g e m e n t programs. A s o n e e x a m p l e , f a c e of t h e integument. Like B.t., t h e s e fungi c a n be t h e NPV f r o m the bollworm, Heliothis zea (Boddie), mass-produced, using fermentation techniques. is registered for use in the U n i t e d States. T h e Their use in Heliothis m a n a g e m e n t is limited p r i m • a d v a n t a g e s of NPVs include their relative host- arily by the length of the incubation period a n d the specificity a n d high virulence. H o w e v e r , they also restricted e n v i r o n m e n t a l conditions that must be

138 present in order for pathogen invasion to o c c u r In field-cage studies, d a m a g e to soybeans a n d ( M c C o y 1974; Bell 1974). corn by H. zea was r e d u c e d by applications of this fungus, with mortality d u e to this pathogen r e a c h • ing 7 6 % (Ignoffo et al. 1978; M o h a m e d et al. 1978). Protozoa: Microsporidia Spp Although epizootics were induced, it w a s c o n - cluded that e c o n o m i c d a m a g e was not prevented, Few protozoan pathogens of insects have b e e n primarily d u e to the relatively long incubation field-tested as microbial agents for c r o p pests, per• period of the infection, a n d it was suggested that N. haps b e c a u s e the incubation period is so long that rileyi w o u l d be useful as a prophylactic agent. crop d a m a g e is usually not controlled ( M c L a u g h l i n In general, the fungi are going to have their great• 1971). Microsporidia have been found to o c c u r in est potential as microbial agents in situations natural field populations of Heliothis, a n d these where the microclimate in the area of the host pathogens are also often transmitted to progeny. provides high humidity with temperatures b e t w e e n Again, their use in microbial control of Heliothis is 20 a n d 30°C, and where moderate feeding by pest limited by the long incubation period, the chronic larvae prior to death c a n be tolerated. rather t h a n acute nature of the disease, a n d the fact Similar results have bee n observed in field trials that they must normally be ingested before they with protozoan pathogens, in that d a m a g e w a s c a n d a m a g e the larvae. incurred even w h e n disease prevalence w a s apparently sufficient. The microsporidian, Vairi- morpha necatrix (Kramer), was evaluated as a Demonstrated Potential of microbial control agent for H. virescens a n d H. zea Microbials in t o b a c c o , soybeans, and s o r g h u m (Fuxa a n d Brooks 1979). In that test, larval infection r e a c h e d We c a n say that all of the microbials that infect 65, 99, and 7 2 % in those crops, respectively, w i t h • Heliothis offer potential for control; indeed, several out adequately reducing c r o p d a m a g e . T h e failure of these pathogens are going to act naturally to to control d a m a g e was attributed to the relatively m a n a g e populations of insects as a part of biologi• long incubation period of the infection. T h e infected cal control in the wild. What we are interested in is larvae eventually died, but not before a lengthy the potential for m a n a g i n g the pathogens to m a x • feeding period. Since the e n t o m o g e n o u s protozoa imize their effect in reducing c r o p d a m a g e by Heli• tend to c a u s e debilitative or chronic infections, othis. Of the microbials m e n t i o n e d , the nuclear their best potential for insect control might be in polyhedrosis viruses a n d the b act erium , Bacillus their effect on subsequent generations. thuringiensis, are currently given the best c h a n c e s Most of the research effort involving microbial of s u c c e s s in most Heliothis m a n a g e m e n t pro• control of Heliothis in the United States has b e e n in grams. This does not m e a n that the other k n o w n the use of B. thuringiensis a n d the NPV from H. zea p a t h o g e n s have less potential for use. It is probable (termed Baculovirus heliothis). T h e s e p a t h o g e n s that in certain situations of crop, climate, a n d pest are registered for use against Heliothis a n d are structures, other p a t h o g e n s are likely to give supe• utilized in limited quantities. Although not yet regis• rior population control. However, in most field trials, tered, the NPV isolated from the alfalfa looper, the viruses a n d bacteria appear to have bee n more Autographs californica (Speyer) ( A c M N P V ) has consistent in their effect, a n d production methods also s h o w n promise for use in controlling H. vires• h a v e b e e n d e v e l o p e d for them. For these reasons, cens. This virus has a wider host range than t h e these microbials are favored f r o m a c o m m e r c i a l Heliothis NPV, infecting several other lepidopteran standpoint. pests (Vail et al. 1970; Vail a n d Jay 1973). T h e potential of microbials, as well as their prob• Field or c a g e tests have been c o n d u c t e d to e v a l • lem areas, may be e x a m i n e d by reviewing s o m e of uate B. thuringiensis a n d Heliothis NPV in c o n t r o l • the reported field investigations involving i n d u c e d ling Heliothis in t o b a c c o , corn, a n d s o y b e a n s or natural epizootics in Heliothis. For e x a m p l e , nat• (Gentry et al. 1969; Ignoffo et al. 1978; O a t m a n et al. ural infections of H. zea a n d the t o b a c c o b u d w o r m , 1970). In general, results of these tests were p r o m • H. virescens by N. rileyi have been reported in corn, ising in that both pathogens c a u s e d significant s o y b e a n s, a n d cotton (Smith et al. 1976). D i s e a s e reductions in plant d a m a g e by Heliothis larvae. p r e v a l e n c e s o m e t i m e s e x c e e d e d 5 0 % during peri• However, the level of control obtained w a s not ods most favorable for development of the disease. effective e n o u g h to c o m p e t e with c h e m i c a l insecti-

139 cides. Although the potential for use on these crop s of the known rapid inactivation of NPV, one possi• obviously exists, further research has been limited. bility explored was of spray formulations that woul d As in other specialized areas of research into improve the persistence of pathogens on field cot• Heliothis management, the majority of work in ton (Yearian and Young 1974; Ignoffo et al. 1976b). microbial control with 8. thuringiensis and NPV has Various formulations were developed that pro• been associated with cotton production. Since the tected the polyhedra from sunlight and increased mid-1960s, considerable testing has been con• the field persistence of the virus (Bull et al. 1976). ducted in the use of these pathogens, resulting in However, the use of these materials failed to signifi• their limited commercial use on cotton. However, cantly increase efficacy. the level of control of Heliothis spp on cotton pro• Since both the NPV and B. thuringiensis must be duced by multiple applications of these microbials ingested, it is important to place the pathogens in has been erratic. This has been especially true of close proximity to the Heliothis larvae. Various NPV. In some tests, control comparable to chemi• methods have been investigated, and their results cal insecticides has been observed. Ignoffo et al. demonstrated the importance of application tech• (1965) reported yields of 560 kg and 715 kg of seed niques (Falcon 1978; Smith et al. 1977a; 1977b). cotton/acre (0.4 ha), respectively, from cotton Improved coverage alone, however, has not plots treated with 6.0 x 1011 and 6.0 x 101 2 p o l y h e d - resulted in sufficient dependability of microbial ral inclusion bodies (PIB) per 0.4 hectare. Yields control to significantly increase its use in Heliothis from untreated plots were 294 kg/0.4 ha. Also, management programs. Allen et al. (1967) found that applications of NPV at Another method of improving the efficacy of 8. 1 1 1.2 x 10 PIBs per 0.4 ha were as effective as a thuringiensis and NPV in the control of Heliothis in toxaphene-DDT standard in small-plot tests. Other cotton has been through the use of gustatory stim• field studies indicated that applications of virus ulant formulations. It has long been recognized that should result in satisfactory control on cotton whe n the effectiveness of these pathogens might be used with the naturally occurring predator-parasite improved through the use of bait-type materials to complexes (Allen et al. 1966). Shieh and Bohmfalk increase larval ingestion of the pathogens (Mon- (1980) found that seed cotton yields increased by toya et al. 1966; McLaughlin et al. 1971; Patti and 10 to 40% over check plots when multiple treat• Carner 1974). Ignoffo et al. (1976a) discussed the ments of the NPV were applied to cotton under a favorable properties of a microbial adjuvant; these relatively low infestation pressure. However, sev• included a feeding stimulant, a sunlight protectant, eral other researchers have obtained marginal or and an evaporation retardant, with the most impor• no control in field tests whenever Heliothis NPV tant of these additions being the feeding stimulant was used alone (McGarr and Ignoffo 1966; McGarr capable of increasing foliar feeding of the larvae. 1968; Pfrimmer 1979). We might also add that the properties of a commer•

In general, the level of control of Heliothis spp in cial adjuvant should further include reasonable cotton obtained with 8. thuringiensis (isolate HD-1) storage and spray characteristics and an economi• has been more consistent than that obtained with cally feasible cost at the projected use rate. NPV. Although the quantity of material used was Here, I would like to discuss my interest and work not economically feasible, control comparable to in the area of microbial control of Heliothis in c o t • chemical insecticides was reported by McGarr et ton. In 1974 and 1975, we conducted field tests to al. (1970). Other field studies have shown that determine the effectiveness of the AcMNPV in a applications of 8. thuringiensis at rates of 3.6 to 7.3 bait formulation for controlling pink bollworms, Pec- x 109 International Units (IU) /0.4 ha will suppress a tinophora gossypiella (Saunders) in cotton (Bell larval population and result in increased yield and Kanavel 1977). Although the microbial formu• (Pfrimmer et al. 1971; Bull et al. 1979; Pfrimmer lation failed to control pink bollworms, the results of 1979). However, the level of control was generally that study again demonstrated the increased effec• less than that obtained with the recommended tiveness of NPV in Heliothis control when applied in c h e m i c a l s . a feeding-stimulant formulation. The percent boll Most recent research in microbial control of Heli- d a m a g e by Heliothis showed 87% reduction in othis has been directed towards developing plots treated with virus in bait, compared with 59% methods or techniques to increase the dependabil- reduction in plots treated with virus alone. How• ity and effectiveness of NPV and 8. thuringiensis. ever, the bait was a liquid formulation, with poor Various possibilities have been explored. Because storage characteristics.

140 In 1976, we began working toward developing a spray adjuvant for use with microbials against Heli- T a b l e 1 . A v e r a g e mortality o f n e o n a t e larvae o f othis in cotton, keeping in mind the properties that tobacco budworms after a 2-hour exposure to cotton a should be incorporated into such an adjuvant (Bell plants treated with NPV In various formulations. and Kanavel 1978). Our first step was to screen Formulation ingredientsb possible ingredients for feeding preference by first M o r t a l i t y ( % w t . i n w a t e r ) ( % a f t e r 1 0 d a y s ) instar H. virescens larvae. A single larva was

allowed to respond either to test material incorpo• W a t e r a l o n e 3 3 . 3 a rated in agar solution or to an agar control. A 5 % c o t t o n s e e d f l o u r 5 1 . 5 a b sequential test for binomial data was used to estab• 1 0 % c o t t o n s e e d f l o u r 6 6 . 7 bc lish limits to accept the hypothesis if 75% of the 5 % c o t t o n s e e d f l o u r larvae responding preferred the treatment, or to 2 % s u c r o s e 6 2 . 2 bc reject it if 25% responded to the control (Ghosh 2 % s u c r o s e 1970). Of the materials screened, cottonseed flour 1 % c r u d e c o t t o n s e e d o i l 6 3 . 8 bc 5 % s o y f l o u r and soy flour appeared the most promising as 2 % s u c r o s e bases for a spray adjuvant. We then conducted a 1 % c r u d e c o t t o n s e e d o i l 7 6 . 0 c d greenhouse study to determine whether the var• 5 % c o t t o n s e e d f l o u r ious stimulants would increase the effectiveness of 2 % s u c r o s e the AcMNPV against neonate H. virescens. T h e 1 % c r u d e c o t t o n s e e d o i l 9 3 . 3 d treatments consisted of virus applied to plants in

water alone and in various combinations of cotton• a . A v e r a g e o f f i v e r e p l i c a t e s w i t h 2 5 t o 3 2 seed flour, cottonseed oil, soy flour, and sucrose. l a r v a e p e r r e p l i c a t e . M e a n s f o l l o w e d b y After the plants had dried, neonate larvae were t h e s a m e l e t t e r d o n o t d i f f e r a t t h e 5 % placed on each and left for 2 hours. The larvae level (Duncan's multiple range test). were then removed, placed in individual diet cups, b . T w e e n 8 0 ( s u r f a c t a n t ) a d d e d ( 0 . 2 6 m l p e r and held to determine the percent viral mortality. In l i t e r ) t o a l l f o r m u l a t i o n s . this test, the percentage of larvae infected was significantly greater when the virus was applied with an adjuvant (Table 1). A mixture containing 5 14 October. parts cottonseed flour (62.5%), 2 parts sucrose The results of this test demonstrated that the (25%), and 1 part crude cottonseed oil (12.5%) was addition of the adjuvant to the virus application prepared and used as the adjuvant in the following significantly increased the percentage of field lar• studies. vae that consumed an infective dose (Table 2). The first field test of this adjuvant was conducted Further, the boll and square damage was signifi• in Phoenix, Arizona, in 1977 on late-planted cotton cantly less in plots treated with virus plus adjuvant (unpublished data). A pretreatment count of 100 than in plots treated with virus alone. In this test, random terminals in the test area showed 356 Heli- application of virus alone did not reduce the dam• othis e g g s ( 9 1 % H. virescens) and 24 first-instar age to squares although it did reduce boll damage. larvae. The treatments consisted of four replicates This was probably due to the rather long incubation each of: virus alone (AcMNPV at 8.9 x 1011 polyhed- period required by the nuclear polyhedrosis virus; ral inclusion bodies [PIB] in 187 liters water/ha), that is, the virus did not act rapidly enough to signifi- virus + adjuvant (8.9 x 1011 PIB + 5.6 kg adjuvant in cantly affect feeding on the squares, but did act to 187 liters water/ha), and an untreated control, in a reduce feeding by larger larvae on bolls. This effect random design. Treatments were applied on 30 demonstrates the need for knowing the growth September, 4 October, and 11 October, using a stage of the crop as well as the size and feeding high-clearance sprayer. The effect of the treat• habits of the larvae during the incubation period of m e n t s on the Heliothis population was evaluated by the proposed microbial control agent. Other possi• collecting five samples of live Heliothis larvae from ble effects of Heliothis control based on the growth each plot during the test period and holding them to stage of cotton were discussed by Falcon (1974). determine mortality caused by the virus. The effect By the 1978 growing season, a commercial com- of the treatments on crop damage was evaluated pany (Traders Oil Mill Co., Fort Worth, Texas) had by c h e c k i n g bolls a n d squares for Heliothis d a m - produced the adjuvant and provided it for our tests age on 50 randomly selected plants in each plot on (trade name: COAX® ). The objectives of our 1978

141 Table 2. Evaluation of microbial treatments on Helio this larvae and cotton plant damage due to Heliothis.

b Heliothis larvae Bollc Squarec infected with d a m a g e d a m a g e a A c M N P V (%) T r e a t m e n t Rate/ha (%) (%)

AcMNPVc 8.9x101 1 P I B

A d j u v a n t 5 . 6 k g 7 6 . 8 c 1 1 . 0 c 2 7 . 8 b

11 A c M N P V 8 . 9 x 10 P I B 4 8 . 6 b 2 1 . 6 b 4 7 . 0 a

U n t r e a t e d 2 . 0 a 3 7 . 4 a 5 1 . 6 a a . Treatments applied in 187 liters water/ha. b . Average of four replicates over five sampling date s with 51 to 98 larvae per sample. c . Average of four replicates with 50 plants per sam ple. Means within columns followed by different letters are significantly different at th e 5% level of confidence (Duncan's multiple range test).

field tests were to evaluate the feeding adjuvant, respectively. We believe that the level of control the NPV from the alfalfa looper, and the HD-1 strain obtained by the pathogen mixture in this study was of S. thuringiensis in controlling H. virescens in equal to the control normally obtained by chemical cotton (Bell and Romine 1980). The tests were insecticides. conducted on cotton planted late to maximize dam• A second test in 1978 was conducted on 0.02-ha a g e by H. virescens. The first test consisted of four plots of late-planted cotton with three treatments- treatments arranged in a Latin-square design with untreated control; B. thuringiensis alone; and B.t. + 0.025-ha plots. The treatments were: untreated, adjuvant—and four replicates. The spray dates and AcMNPV alone, AcMNPV + adjuvant, and AcMNPV methods of evaluation were the same as in the + 8. thuringiensis + adjuvant. A total of eight appli• above test. Also, the numbers of Heliothis eggs a n d cations was made between 1 September and 15 larvae found on terminals were similar. No differen• October and an application of malathion was made ces in the numbers of eggs per plant were ever on 4 September to reduce levels of predators and noted among the treatments. parasites to insure maximum Heliothis d a m a g e . As in our previous studies, the addition of the We evaluated the treatments by periodically exa• adjuvant increased the effectiveness of the patho• mining 10 randomly selected plants/plot. The data gen in controlling Heliothis. Square damage during recorded were: number of Heliothis eggs per termi• the test period 6 September to 19 October was nal; total number of bolls and squares; and the 8.8% with 8. thuringiensis + adjuvant; 18.3% with 8. number of bolls and squares damaged by Heliothis. thuringiensis alone, and 44.5% in untreated plots. Further, the effect on yield was determined by harv• The difference in yield (Table 4) in cotton plots esting 15 row m/plot at the end of the season. treated with B. thuringiensis + adjuvant mixture In this test, the average number of Heliothis e g g s represented a 32% increase over plots treated with ( 9 3 % H. virescens) ranged from four to six per B. thuringiensis alone. terminal during the treatment period. Treatment In these tests, the mixture of bacillus and virus with the mixture of AcMNPV + B. thuringiensis + appeared to give more efficacious control than the adjuvant resulted in the best control, regardless of other treatments, even though these two patho• the method of evaluation. The yield of cotton gens are antagonistic in laboratory bioassay stu• obtained using this treatment (Table 3) was as dies (M.R. Bell, unpublished data). We felt that good as could be expected for a late-planted crop. possibly the sublethal effect of B. thuringiensis The seasonal averages of percent damaged (reduced growth rate) as described by Dulmage et squares in plots treated with NPV + B. thuringiensis al (1978) was involved; that is, the larvae, although + adjuvant, NPV + adjuvant, NPV alone, and in not rapidly killed by the virus, remain small becaus e untreated plots were 6.1, 14.5, 28.2, and 43.0%, of the stunting effect of B. thuringiensis during the

142 T a b l e 3 . Y i e l d i n l a t e - p l a n t e d c o t t o n t r e a t e d w i t h m i c r o b ials for control of Heliothis.a

b T r e a t m e n t Rate per ha Yield seed cottonc

Bacillus thuringiensis 5 6 0 g 1 4 2 7 a A c M N P V 7 . 4 1 x 1011 P l B A d j u v a n t 3 . 3 6 k g

A c M N P V 7 . 4 1 x 1011 P l B 1 0 6 6 b A d j u v a n t 3 . 3 6 k g

A c M N P V 7 . 4 1 x 1011 P l B 7 7 4 c

Untreated control 3 3 2 d a . Average of four replicates, 15 row meters hand-pi cked per replicate. b . All treatments applied in 93.5 liters water/ha. c . Means within columns followed by different letters are significantly different at the 5% level of confidence (Duncan's multiple range test—A NOV of latin square).

T a b l e 4 . Y i e l d i n l a t e - p l a n t e d c o t t o n t r e a t e d w i t h Bacillus thuringlensis for control of Heliothis.a

b T r e a t m e n t Rate/ha Yield seed cottonc

Bacillus thuringiensis 5 6 0 g 1 1 0 8 a A d j u v a n t 3 . 3 6 k g

B. thuringiensis 5 6 0 g 8 3 7 b

Untreated control 3 2 8 c a . Average of four replicates—1 5 row meters hand-pic ked per replicate. b . All treatments applied in 93.5 liters water. c. Means within columns followed by different lette rs are significantly different at the 5% level of confidence (Duncan's multiple range test).

incubation period, resulting in less feeding dam• tend to increase the probability that Heliothis s p p age. Although much is still unknown regarding the larvae will ingest an active microbial at the proper most efficient use of these methods, we feel that time have been relatively consistent in increasing the mixture of NPV and B. thuringiensis will find a the effectiveness and level of control. These proce• place in future Heliothis management in cotton. We dures have included the use of feeding stimulants, have also been further encouraged by the promis• optimum dosages, spray methods that result in ing results of other researchers using such mix• maximum deposits in the target area, and proper tures (Ummel 1981), and by the increasing quantity timing of the application, so that it affects larvae as of annual sales of the adjuvant (over $1 million). early as possible (Falcon 1971; Chapman and In summary, I feel that the potential exists for Ignoffo 1972; Stacey et al. 1977). microbial control of Heliothis in almost any crop Obviously, climate can have much to do with the and any location. However, methods and microb• probability of successfully inducing an epizootic, ials must be utilized to maximize their best features, not only by its effect on the inactivation of the based upon the characteristics of the crop, larval microbial or climatic requirements for infection, but feeding habits, pathogen and disease symptoma• also physical actions such as washing the microb• tology, and climate. For example, procedures that ials from the target area by frequent rainfall.

1 4 3 Although we have learned much, and have pro• BULL, D.L., RIDGWAY, R.L., HOUSE, V.S. and gressed somewhat in the area of microbial control PRYOR, N.W. 1976. Improved formulation of the Helio• of Heliothis, much research remains to be con• this nuclear polyhedrosis virus. Journal of Economic Entomology 69: 731 -736. ducted before the potential that was envisioned for

insect pathogens is even partially realized. The CHAPMAN, A.J., and IGNOFFO. C.M. 1972. I n f l u e n c e development and evaluation of insect pathogens of rate and spray volume of nucleopolyhedrosis virus o n requires adequate funding, which generally has not control of Heliothis in cotton. Journal of Invertebrate been available. Even without increased funding, Pathology 20:183-186. the use of microbial control should increase, DULMAGE, H.T., GRAHAM, H.M., and MARTINEZ, E. though at a slower rate. Many efforts are being 1 9 7 8 . Interactions between the tobacco budworm, Helio• made to increase the effectiveness and use of this virescens, and the endotoxin produced by the HD-1 microbial agents in insect pest management by isolate of Bacillus thuringiensis var. Kurstaki: relationship isolating and identifying new, more virulent patho• between length of exposure to the toxin and survival. gens; improving methods of pathogen production; Journal of Invertebrate Pathology 32: 40-50. improving spray formulations and techniques; and FALCON, L.A. 1971. Microbial control as a tool in inte• determining plant-insect-pathogen interactions. grated control programs. Pages 346-364 i n Biological The successful development of more effective control, ed. C.B. Huffaker New York. USA: Plenum Pr e s s methods, coupled with the user's increased knowl- FALCON, L.A. 1974. Insect pathogens: integration intoa edge of factors involved in microbial control, should pest management system. Pages 618-627 i n P r o c e e d • result in more reliable usage of pathogens in Helio- ings, Summer Institute on Biological Control of Plant this management. Insects and Diseases. Jackson, Miss, USA: Universit y Press of Mississippi.

FALCON, L.A. 1978. Application technology: improving References coverage with microdroplet applicators. Pages 113-1 1 7 in Proceedings, Microbial Control of Insect Pests: Fu t u r e ALLEN, G.E., GREGORY, B.G., and BRAZZEL, J.R. Strategies in Pest Management Systems. University of 1 9 6 6 . Integration of the Heliothis nuclear polyhedrosis Florida, Gainesville, Fla, USA. virus into a biological control program for cotton J o u r n a l FUXA, J.R., and BROOKS, W.M. 1979. Effects of Vairi- of Economic Entomology 59: 1333-1336. morpha necatrix in sprays and corn meal on Heliothis ALLEN, G.E. GREGORY, B.G., and PATE, T.L. species in tobacco, soybeans, and sorghum. Journal o f 1 9 6 7 . Field evaluation of a nuclear polyhedrosis virus in Economic Entomology 72:462-467. the control of Heliothis zea a n d Heliothis virescens on GENTRY, C.R., THOMAS, W.W., and STANLEY, J.M. cotton. Journal of Invertebrate Pathology 9: 40-42. 1969. Integrated control as an improved means of BELL, J.V. 1974. Mycoses. Pages 185-236 i n I n s e c t reducing populations of tobacco pests. Journal of E c o • diseases, Volume 1, ed. G.E. Cantwell. New York, US A: nomic Entomology 62: 1274-1277. D e k k e r . GHOSH, B.K. 1970. Sequential tests of statistical BELL, M.R., and KANAVEL, R.F. 1977. Field tests of a hypothesis. Reading, Mass, USA: Addison Wesley. 454 nuclear polyhedrosis virus in a bait formulation for c o n t r o l pp. of pink bollworms and Heliothis spp. on cotton in Arizona. IGNOFFO, C.M., CHAPMAN, A.J., and MARTIN, D.F. Journal of Economic Entomology 70: 625-629. 1965. The nuclear polyhedrosis virus of Heliothis zea BELL, M.R., and KANAVEL, R.F. 1978. Tobacco bud- (Boddie) and Heliothis virescens (Fabricius). III. The worm: development of a spray adjuvant to increase e f f e c • effectiveness of the virus against field population s of H e l i - tiveness of a nuclear polyhedrosis virus. Journal of othis on cotton, corn and grain sorghum. Journal of Inver- Economic Entomology 71: 350-352. tebrate Pathology 7:227-235.

BELL, M.R., and ROMINE, C.L. 1980. Tobacco budworm: field evaluation of microbial control in cott o n u s i n g IGNOFFO, C.M., HOSTETTER, D.L., and SMITH, D.B. Bacillus thuringiensis and a nuclear polyhedrosis virus 1 9 7 6 a . Gustatory stimulant, sunlight protectant, evapo• with a feeding adjuvant. Journal of Economic Entomo l o g y ration retardant: three characteristics of a microb i a l 73: 427-430. insecticidal adjuvant. Journal of Economic Entomolo g y 69:207-210. BULL, D.L., HOUSE, V.S., ABLES, J.R., and MORRI• SON, R.K. 1979. Selective methods for managing insect IGNOFFO, C.M., YEARIAN, W.C., YOUNG, S.Y., pests of cotton. Journal of Economic Entomology 72: HOSTETTER, D.L., and BULL, D.L. 1976b. Laboratory 8 4 1 - 8 4 6 . and field persistence of new commercial formulation s o f

144 t h e Heliothis nucleopolyhedrosis virus, Baculovirus helio- biological insecticides. Journal of Economic Entomo l o g y this. Journal of Economic Entomology 69: 233-236. 72: 593-598.

IGNOFFO, C.M., HOSTETTER, D.L., BIEVER, K.D., PFRIMMER, T.R., FURR, R.E., and STADELBACHER, GARCIA, C., THOMAS, G.D., DICKERSON, W.A., and E.A. 1 9 7 1 . Materials for control of boll weevils, boll- PINNELL, R. 1978. Evaluation of an entomopathogenic worms, and tobacco budworms on cotton at Stoneville, bacterium, fungus, and virus for the control of Heliothis Mississippi. Journal of Economic Entomology 64: 475 - zea on soybeans. Journal of Economic Entomology 71: 4 7 8 . 1 6 5 - 1 6 8 . SHIEH, T.R., and BOHMFALK, G.T. 1980. Production McCOY, C.W. 1974. F u n g a l p a t h o g e n s a n d their u s e i n and efficacy of baculoviruses. Biotechnology and Bioe n - the microbial control of insectsand mites. Pages 564- 5 7 5 gineering22: 1357-1375. in Proceedings, Summer Institute on Biological Control of SMITH, D.B., HOSTETTER, D.L., and IGNOFFO, C.M. Plant Insects and Diseases. Jackson, Miss, USA: Univ e r • 1 9 7 7 a . Laboratory performance specifications for a bac- sity Press of Mississippi. terial (Bacillus thuringiensis) a n d a viral (Baculovirus heli- McGARR, R.L. 1968. Field tests w i t h a n u c l e a r p o l y h e d • othis) insecticide. Journal of Economic Entomology 70: ral virus against the bollworm and tobacco budworm, 4 3 7 - 4 4 1 . 1964-1966. Journal of Economic Entomology 61: 342. SMITH, D.B., HOSTETTER, D.L., and IGNOFFO, C M . McGARR, R.L., DULMAGE, H.T., and WOLFEN- 1977b. Ground spray equipment for applying Bacillus BARGER, D.A. 1970. T h e δ - e n d o t o x i n of Bacillus thu- thuringiensis suspension on soybeans. Journal of Eco- ringiensis, HD-1, and chemical insecticides for control of nomic Entomology 70: 633-637. t h e t o b a c c o b u d w o r m a n d t h e b o l l w o r m . J o u r n a l o f E c o • SMITH, J,W., KING, E.G., and BELL, J.V. 1976. P a r a s - nomic Entomology 63: 1357-1358. ites and pathogens among Heliothis s p e c i e s i n t h e C e n • McGARR, R.L., and IGNOFFO, C.M. 1966. Control of tral Mississippi delta. Journal of Economic Entomol o g y 5: Heliothis spp. with a nuclear polyhedrosis virus, EPN. and 2 2 4 - 2 2 6 . two newer insecticides. Journal of Economic Entomolog y STACEY, A.L., YOUNG, S.Y., III, and YEARIAN, W.C. 59: 1284-1285. 1 9 7 7 . Effect of larval age and mortality level on damage MCLAUGHLIN, R.E. 1971. Use of protozoans for to c o t t o n by Heliothis zea i n f e c t e d w i t h Baculovirus helio- microbial control of insects. Pages 151 -172 in M i c r o b i a l this. Journal of Economic Entomology 70: 383-386. control of insects and mites, eds. D. Burges and N.W. UMMEL, E. 1981. Elcar a n d T h u r i c i d e H P c o m b i n a t i o n Hussey. New York, USA: Academic Press. for the c o n t r o l of the t o b a c c o b u d w o r m in c o t t o n in t h e

McLAUGHLIN, R.E., ANDEREWS, G.L., and BELL, Southwest. Pages 82-86 in Proceedings, Conference on M.R. 1 9 7 1 . Field tests for c o n t r o l of Heliothis spp. w i t h a Biological Control on Cotton, Dallas, Tex, USA. San nuclear polyhedrosis virus included in a boll weevil bait. Diego, Cal: Sandoz. Journal of Invertebrate Pathology 18: 304-305. VAIL, P.V., and JAY, D.L. 1973. Pathology of a nuclear MOHAMED, A.K.A., BELL. J.V., and SIKOROWSKI, p o l y h e d r o s i s virus of t h e alfalfa looper in alternate h o s t s . P.P. 1 9 7 8 . Field c a g e tests with Nomuraea rileyi against Journal of Invertebrate Pathology 21: 198-204. corn earworm larvae on sweet corn. Journal of Economic VAIL, P.V., JAY, D.L., and HUNTER, D.K. 1970. C r o s s Entomology 71: 102-104 infectivity of a nuclear polyhedrosis virus isolated f r o m t h e MONTOYA, E.L., IGNOFFO, C.M., and McGARR, R.L. alfalfa looper, Autographa californica. Pages 297-304 in 1 9 6 6 . A feeding stimulant to increase effectiveness of, Proceedings, Fourth International Colloquium on Insect and a field test with a nuclear polyhedrosis virus of Helio• Pathology, this. Journal of Invertebrate Pathology 8: 320-324. YEARIAN, W.C, and YOUNG, S.Y. 1974. Persistence OATMAN, E.R., HALL, I.M., ARADAWA, K.Y., of Heliothis nuclear polyhedrosis virus on cotton plant PLATNER, G.R., BASCOM, L.A., and BEEGLE, C.C. parts. Environmental Entomology 3:1035-1036. 1 9 7 0 . C o n t r o l o f t h e c o r n e a r w o r m o n s w e e t c o r n i n S o u t h e r n C a l i f o r n i a w i t h a n u c l e a r p o l y h e d r o s i s virus a n d Bacillus thuringiensis. Journal of Economic Entomology 63: 415-421.

PATTI, J.H., and CARNER, G.R. 1974. Bacillus thurin• giensis investigations for control of Heliothis s p p . on c o t • ton. Journal of Economic Entomology 67: 415-418.

PFRIMMER, T.R. 1979. Heliothis spp. control on cotton with pyrethroids, carbamates, organophosphates, and

145

Possibilities for Natural Enemies in Heliothis Management and the Contribution of the Commonwealth Institute of Biological Control

D.J. Greathead and D.J. Girling*

Abstract

Some factors affecting the efficiency of natural enemies as control agents for Heliothis spp are discussed, notably the effects of migration, feeding behavior, host plant, climate, and insecticide usage. Although a large number of insect natural enemies have been reported, only a few in each region are sufficiently abundant to be of interest as control agents. Re• cent research on natural enemies in the main areas where H e l i o t h i s spp are major pests is briefly reviewed and discussed in relation to the possibilities tor their application in bio• logical and integrated pest control by introduction or conservation. It is concluded that patho• gens are only likely to be useful when applied as biological pesticides, and that predators are best manipulated by conservation and augmentation. On the other hand, there are possi• bilities for the introduction of insect parasitoids to occupy empty niches in some areas and tor their conservation and augmentation in pest-management schemes. However, knowledge is at present insufficient to make full use of natural enemies. Further surveys are likely to re• veal additional useful species, especially in South America, and in all areas quantitative ecological studies backed by investigations on the biology of the more important species of natural enemies are required before substantial progress can be made. The Commonwealth Institute of Biological Control, backed by the information and identification services of the Commonwealth Agricultural Bureaux, is able to assist in furthering these objectives.

*Commonwealth Institute of Biological Control, Imperial College, Silwood Park, Ascot, Berks, UK,

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. 147 Heliothis spp are important pests in a l m o s t all w a r m A g a i n , there is little firm e v i d e n c e available, but it t e m p e r a t e a n d tropical countries. T h e s p e c i e s i n seems likely that unnaturally large fruits and other e a c h a r e a are closely related a n d are p o l y p h a g o u s , plant o r g a n s in m a n y c r o p plants e n a b l e pest lar• a l t h o u g h e a c h has preferred host plants. Usually, v a e t o e s c a p e ovipositing parasitoids, b e c a u s e they f o r m part of a c o m p l e x of pests that must be they b u r r o w out of range of ovipositors e v o l v e d to i n c l u d e d i n a n y m a n a g e m e n t p r o g r a m ; therefore, reach hosts in less fleshy wild progenitors of crop they are not ideal targets for "classical" biological plants. control, but natural enemies are important mortality f a c t o r s a n d s h o u l d play a part in any m a n a g e m e n t scheme. This paper reviews the possibilities for Crop and Natural Enemy enhancing natural enemy mortality, especially by a r t h r o p o d parasitoids a n d predators, a n d outlines The natural enemy spectrum on particular crops is the possible contributions of the Commonwealth not only a c o n s e q u e n c e of host behavior but also of Institute of Biological Control (CIBC). t h e s e a r c h i n g behavior of the natural e n e m i e s a n d their microenvironmental preferences. For exam• Host Biology and Natural Enemies ple, Eucelatoria sp is m o r e strongly attracted to the host plant t h a n to H. virescens, a n d okra is m o r e A number of biological features of Heliothis s p p strongly attractive than cotton (Nettles 1979). Even affect the prospects of biological control and need if the host is successfully parasitized on a particular to be kept in m i n d in c o n s i d e r i n g t h e likely effective• host plant, t h e parasitoid m a y fail to survive; thus ness of biotic control agents. Hyposoter exiguae larvae in H. zea feeding on Although diapause is widespread, the proportion t o m a t o are p o i s o n e d by t o m a t i n e present in the of d i a p a u s i n g p u p a e t e n d s to i n c r e a s e f r o m zero in host haemolymph (Campbell and Duffey 1979). populations near the equator, w h e r e c o n t i n u o u s O t h e r plant d e f e n s e s m a y affect the parasite b r e e d i n g is possible, to c l o s e on 1 0 0 % in p o p u l a • directly. B h a t n a g a r (1980) notes that H. armigera tions f r o m t e m p e r a t e regions at t h e e n d of the e g g s on c h i c k p e a a n d p i g e o n p e a at ICRISAT are f a v o r a b l e s e a s o n . H. armigera a n d H. zea are not parasitized a n d that with c h i c k p e a , at any rate, k n o w n migrants of the northern fringe of their this may come about because parasite adults are r a n g e s , but the d e g r e e to w h i c h they migrate e l s e • t r a p p e d by the sticky exudation on the plant sur• where is controversial. Recent trapping studies in f a c e . T h e s e recent discoveries begin to explain the A f r i c a ( B o w d e n 1973) a n d India ( B h a t n a g a r 1980), c o m p l e x factors that a c c o u n t for the m a n y i n w h i c h c a t c h h a s b e e n related t o weather, h a v e o b s e r v e d d i f f eren c e s in the parasite s p e c t r u m of led s o m e entomologists to assert that H. armigera Heliothis s p p on different host plants. is m o r e mobile t h a n has b e e n realized a n d that it is Another factor that affects biological control of at least a partial migrant throughout its range. Other pests of annual c r o p s is the timing of c r o p d a m a g e e n t o m o l o g i s t s are sceptical. H o w e v e r , in a r e a s in relation to s e a s o n . T h u s , c r o p s g r o w n early in the w h e r e H. armigera c a n be s h o w n to be migrant, s e a s o n m a y be m o r e severely a f f e c t e d t h a n later biological control will be less easy to achieve, as plantings where time is required for natural ene• resident natural e n e m i e s are unlikely to be able to mies to build up n u m b e r s from low o f f - s e a s o n lev• respond effectively to a sudden influx of ovipositing els. In some instances, natural enemies only m o t h s . b e c o m e effective during the last pest g e n e r a t i o n — The possibility that some natural enemies are t o o late to be of any value. H e a v y pesticide u s a g e is also migrant has hardly b e e n investigated but a further factor affecting biological control pros• s h o u l d be e x p l o r e d . Certainly s o m e g r o u p s of p a r a - pects; thus Carl (1977) notes that the natural- sitoids, e.g., I c h n e u m o n i d a e or O p h i o n i n a e , are enemy complex of Heliothis s p p on agricultural periodically a b u n d a n t i n light-trap c a t c h e s , w h i c h c r o p s i n E u r o p e a n d N o r t h A m e r i c a h a s b e e n dras• is s u g g e s t i v e of migration. tically r e d u c e d , probably as a result of the t e n d e n c y T h e Heliothis larva's habit of boring into fruits, towards monocultures, pollution with increasingly maize c o b s , buds, a n d other plant o r g a n s gives m o r e powerful insecticides, a n d the extensive use partial protection from natural enemies and redu• of herbicides. He queries the value of s e a r c h i n g for ces the likelihood of effective biological control in natural e n e m i e s on n on c u l t i v at e d plants. If t h e s e c r o p s w h e r e the larvae are not f e e d i n g o n t h e " w e a k e r " links of the c o m p l e x h a v e b e e n f o r c e d out surface. of agricultural areas because of environmental

148 pressures, it is unlikely that they can be reestab• India lished, unless integrated control measures enhance their chances of survival. Extensive studies on natural enemies of H. armig• era, chiefly in Karnataka, were made by the Indian Station of CIBC during the 1960s for the U.S. PL- 480 project. Eight important parasites of the larvae Parasitoids and Predators and pupae were recognized (Achan et al. 1968; Rao 1968), some of which were shipped to the USA and tested on H. zea (Table 1), but only Palexorista Large numbers of insect natural enemies of Helio• laxa and two egg parasitoids bred on this species this spp have been reported wherever studies have (Manjunath 1972). Since 1974, studies have been been made, but most of those listed are incidental, m a d e on Heliothis spp by ICRISAT (Bhatnagar contributing little to overall mortality. For examp l e , 1980), indicating a similar complex in Andhra Pra• Achan et al. (1968) list 37 species of insect parasi • desh and emphasizing the influence of the host toids of H. armigera in India, of which only eight plant on the relative abundance of different were classed as important (each achieving over species. 3% parasitism). Only "important" species—i.e., A program for introduction of parasitoids from the those consistently present and capable of causing USA started in 1976 at the Central Biological Con• significant mortality—are of interest, and only these trol Station, Bangalore, assisted by the CIBC will be discussed further. (Nagarkatti, these Proceedings).

Europe and the USSR Africa

Detailed studies of natural enemy mortality of H. A recent survey by Carl (1977, 1978) in southern armigera have been made by entomologists prim• Europe and Morocco, where Heliothis armigera is arily interested in its control on cotton (Parsons resident, has shown that the diversity of parasite 1940, in South Africa; Coaker 1959, in Uganda; and complexes is very reduced. Nonetheless, substan• Reed 1965, in Tanzania). Many other records have tial rates of parasitism were found in southeastern been published, but are unreliable or fragmentary Europe and Morocco. On tobacco in Bulgaria, Hyp- (see Greathead 1966 for a list of records). The osoter didymator (Thunb.) (Ichneumonidae) and more important parasites are listed in Table 2. Par- Apanteles kazak Telenga (Braconidae) together sons noted that high egg parasitism had little effect achieved rates of parasitism of 41 to 75% on the on the larval population and that overall mortality last host generation. In Morocco, A. kazak a n d was highest on cotton; Coaker, that in an area of possibly other Apanteles spp achieved 15 to 65% relatively uniform rainfall and no severe dry season, parasitism, the rate apparently increasing with host overall parasitism was low, but so was host density; density in a highly polluted environment. Reed, that following the dry season parasitism was Recent studies in cotton fields in Israel have low, built up too late to prevent serious damage to confirmed the importance of Hyposoter didymator, cotton, and reached a peak at the end of the sea• as it has been shown to be the most important biotic son on pigeonpea. The impression gained is that in limiting factor on populations of Heliothis armigera Africa severe dry seasons break synchronization of (Bar et al. 1979). parasite with host, thus preventing parasites becoming effective until most crops have suffered Earlier studies in Turkmenia (Bogush 1957) severe damage. detected 22 parasites, of which the most important were external Bracon spp. (B. brevicornis W e s m . , 6. hebetor Say, 8. smirnovi [Kok.], a n d 8. turkesta- nicus [Telenga]), which are effective on cotton The USA where they build up early in the season on Spodop- tera exigua (Hbst.). Also important were Therion The bollworm complex on cotton in the USA con• (Exochilum) sp on cotton and lucerne; Litomastix sists of Heliothis zea a n d H. virescens, w h i c h is also sp on lucerne, tomato, and chickpea; and Apan• a pest of tobacco. The relative abundance of the teles kazak on tomato. two species varies with locality and time of year,

149 Table 1. Important parasites of Heliothis a r m i g e r a I n I n d i a .

Heliothis s t a g e a f f e c t e d P a r a s i t e a n d p e r c e n t a g e p a r a s i t i z e d

Hymenoptera

Ichneumonidae Banchopsis ruficornis ( C a m . ) L a r v a e , 1 0 % n o h y p e r p a r a s i t e s Campoletis chlorideae Uchidaa Y o u n g l a r v a e , 1 0 - 8 0 % ; hyperparasites Enicospilus spa O l d l a r v a e , 6 - 1 1 % Eriborus spa Y o u n g l a r v a e 3 - 6 % ; n o h y p e r p a r a s i t e s

B r a c o n i d a e

Brecon brevicornis W e s m . L a r v a e , 3 - 6 %

Trichogrammatidae

Trichogramma chilonis I s h i i ( c o n f u s u m V i g g i a n i ) E g g s , t o 7 9 % Trichogrammatoidea armigera N a g a r a j a E g g s , t o 1 1 %

D i p t e r a

T a c h i n i d a e Palexorista laxa (Curran)a O l d l a r v a e , 1 2 - 1 8 % ( m i s i d e n t , a s Drino imberbis W i e d . ) n o h y p e r p a r a s i t e s Carcelia illota (Curran)a O l d l a r v a e 4 - 1 6 % hyperparasites Goniophthalmus h a l l i M e s n i l O l d l a r v a e , 1 8 - 2 0 %

S o u r c e s : A c h a n e t a l . ( 1 9 6 8 ) a n d M a n j u n a t h ( 1 9 7 2 ) . a . S h i p p e d t o t h e U S A a n d t e s t e d o n H . zea; o n l y P . laxa was successfully bred.

a n d is influenced by t h e availability of alternative spp. S o m e of the parasites (Table 4), s u c h as the host plants ( L i n c o l n 1972). Both w e r e minor pests b r a c o n i d s Cardiochiles nigriceps a n d Microplitis of c o t t o n before 1945 a n d w e r e easily controlled by croceipes, are m o r e specific a n d attack the w h o l e t h e synthetic o r g a n i c insecticides that a p p e a r e d r a n g e of larval sizes. T h e c o m p o s i t i o n of t h e natural after the war, but i n c r e a s i n g resistance a n d d e s • e n e m y c o m p l e x varies with location, crop, a n d truction of natural e n e m i e s eventually led to a spiral s e a s o n . of i n c r e a s e d pesticide usage, e n v i r o n m e n t a l pollu• B e c a u s e of the high d e g r e e of natural control, tion, s e c o n d a r y pest outbreaks, a n d disastrous e m p h a s i s i s n o w p l a c e d o n t h e c o n s e r v a t i o n a n d c r o p losses, a n d to n e w r e s e a r c h into the Heliothis a u g m e n t a t i o n of natural e n e m i e s . R e c e n t w o r k p r o b l e m . (e.g. Plapp a n d Vinson 1977), h a s s h o w n that the Natural e n e m i e s are c a p a b l e of exerting f r o m 50 parasitoids c a n b e m u c h m o r e a d v e r s e l y a f f e c t e d to 9 0 % control of t h e Heliothis population ( R i d g w a y b y insecticides t h a n t h e b o l l w o r m s , a n d r e d u c t i o n a n d L i n g r e n 1972). Several h u n d r e d s p e c i e s h a v e in t h e a m o u n t s of insecticides u s e d by setting real- b e e n r e c o r d e d , but f e w e r t h a n 3 0 a r e important. istic d a m a g e thresholds is of primary i m p o r t a n c e in T h e predators ( T a b l e 3 ) usually attack t h e e g g s conserving the natural enemy complex (Newsom a n d smaller larvae, a n d n o n e is specific to Heliothis 1972). S t r i p - c r o p p i n g e x p e r i m e n t s h a v e s h o w n

150 Table 2. Important parasites of H e l i o t h i s armigera In South Africa, Uganda, and Tanzania.

Heliothis s t a g e P a r a s i t e C r o p a f f e c t e d C o u n t r y

Ichneumonidae Charops sp I Legumes, etc. L a r v a e T a n z a n i a Charops sp II C o t t o n L a r v a e U g a n d a Enicospilus sp ? communis S z e p l . C o t t o n L a r v a e U g a n d a

B r a c o n i d a e Apanteles rnaculitarsis C a m . C o t t o n L a r v a e South Africa Apanteles s p ultor g r o u p C o t t o n L a r v a e U g a n d a Apanteles s p n r aethiopicus W i l k P e a s L a r v a e South Africa Bracon ?brevicornis W e s m . Cotton, etc. L a r v a e South Africa Cardiochiles nigricollis ( C a m . ) Cotton, etc. L a r v a e South Africa C. trimaculatus ( C a m . ) C o t t o n L a r v a e U g a n d a Chelonus curvimaculatus C a m . M a i z e L a r v a e South Africa

Trichogrammatidae Trichogrammatoidea sp C o t t o n E g g s South Africa

Scelionidae Phanurus s p . Winter crops E g g s South Africa Telenomus ullyetti N i x o n Winter crops E g g s South Africa C i t r u s E g g s South Africa

T a c h i n i d a e Pa lexorista laxa ( C u r r a n ) C o t t o n L a r v a e T a n z a n i a ( D r i n o imberbis [ w i e d . ] ) South Africa Goniophthalmus h a l l i M e s n i l C o t t o n L a r v a e / T a n z a n i a p u p a e

Sources: Parsons (1940); Coaker (1959); Reed (1965) .

that planting s o r g h u m with cotton e n c o u r a g e s losses of the cotton c r o p in the mid-1950s, as in the beneficial insects and reduces damage (Robinson USA. As a result, an integrated control p r o g r a m et al. 1971). Inundative releases of laboratory- w h i c h included c h a n g e s in cultural practices, c o n • reared natural e n e m i e s at the correct time c a n also servation of natural enemies, a n d the m i n i m u m use be effective, e.g., releases of Chrysopa carnea lar• of insecticides, was developed (Doutt a n d Smith vae at a rate of 292 0 0 0 / a c r e (approximately 7 2 0 1971). Among the natural enemies of H. virescens 0 0 0 / h a ) r e d u c e d Heliothis populations by up to in South A m e r i c a are several tachinids w h i c h , 9 6 % a n d tripled cotton yields (Ridgway a n d J o n e s although not specific to Heliothis spp, play an 1969). D e v e l o p m e n t of c o t t o n varieties with a important part in its natural control (Cortes, unpub• shorter fruiting c y c l e a n d s o m e resistance to Helio- lished). Since s o m e of them belong to e n d e m i c this w o u l d r e d u c e d a m a g e , a n d resistance to other neotropical genera, they offer a possibility for intro• pests w o u l d help r e d u c e the a m o u n t of insecticide duction into other areas. u s e d ( N e w s o m 1972). In the West Indies, braconid parasites of H. zea a n d H. virescens play only a small part in control, but Trichogramma spp and general predators have South and Central America s o m e effect (Bennett a n d Y a s e e n 1972). In 1971 In t h e c o a s t a l valleys of Peru, increasing reliance Campoletis chlorideae a n d Trichogrammatoidea on insecticides after the war led to disastrous armigera were sent to Trinidad f r o m India a n d

151 T a b l e 3 . C o m m o n p r e d a t o r s o f H e l i o t h i s s p p I n t h e U n i t e d S t a t e s o f A m e r i c a .

Heliothis s t a g e P r e d a t o r p r e y e d u p o n

H e m i p t e r a L y g a e i d a e Geocoris punctipes ( S a y ) E g g s , s m a l l l a r v a e

N a b i d a e Nabis ferus ( L . ) Eggs, small/medium larvae N. alternatus P a r s h l e y Eggs, small/medium larvae

Anthocoridae Orius insidiosus ( S a y ) E g g s , s m a l l l a r v a e O. tristicolor ( W h i t e ) E g g s , s m a l l l a r v a e

N e u r o p t e r a Chrysopidae Chrysopa carnea S t e p h . Eggs, small/medium larvae C. oculata S a v Eggs, small/medium larvae C. rufilabris B u r m . Eggs, small/medium larvae

C o l e o p t e r a Coccinellidae Coleomegilla maculata (Deg.) E g g s , s m a l l l a r v a e Hippodamia convergens ( G u e r . ) E g g s , s m a l l l a r v a e Scymnus s p p E g g s , s m a l l l a r v a e

A r a n e i d a A r g i o p i d a e Small/medium larvae O x y o p i d a e Small/medium larvae S a l t i c i d a e Eggs, small/medium/large larvae T h o m i s i d a e Small/medium larvae

S o u r c e : R i d g w a y a n d L i n g r e n 1 9 7 2 .

release d on various islands, but so far there h a v e as is present e l s e w h e r e . T h e predators include the b e e n no reports of establishment. usual r a n g e of p o l y p h a g o u s arthropods, but c o c c i - nellids, present in Q u e e n s l a n d , w e r e not r e c o r d e d in N e w South W a l e s . Australasia In N e w Z e a l a n d , w h e r e larval parasites are absent, a biological control p r o g r a m is being c o n • In Australia, studies on natural e n e m i e s of Heliothis d u c t e d against H. armigera, b a s e d on parasitoids armigera a n d H. punctigera in t h e c o t t o n a g r o e c o - f r o m Europe. T h e t w o parasitoids r e c o m m e n d e d b y s y s t e m b e g a n during t h e last d e c a d e a n d f e w Carl (1977), Hyposoter didymator a n d Apanteles results h a v e b e e n p u b l i s h e d a s yet. R o o m (19 79) kazak are readily c u l t u r ed a n d d i a p a u s e c a n be lists 16 parasitoids a n d 24 predators in t h e N a m o i a v o i d e d , w h i c h e a s e s t h e transfer f r o m t h e N o r t h • Valley, N e w S o u t h W a l e s , but d o e s not indicate e r n H e m i s p h e r e to the S o u t h e r n H e m i s p h e r e . A. their relative i m p o r t a n c e , a n d a list for s o u t h e a s t kazak h a s b e e n s u c c e s s f u l l y c u l t u r e d in N e w Z e a • Q u e e n s l a n d i s provided b y B i s h o p a n d B l o o d land, a n d a release p r o g r a m c a r r i e d out. T h e first (1977). T h e parasitoids in b o t h a r e a s a r e similar r e c o v e r i e s h a v e n o w b e e n m a d e . Unfortunately, (Table 5 ) a n d c o m p r i s e m u c h t h e s a m e s p e c t r u m t h e c u l t u r e of H. didymator w a s lost, but r e i n t r o d u c -

152 T a b l e 4. P r i n c i p a l p a r a s i t e s of Heliothis spp in the U n i t e d S t a t e s of A m e r i c a .

P a r a s i t e Heliothis s t a g e p a r a s i t i z e d

Hymenoptera Ichneumonidae

Campoletis flavicincta ( A s h m . ) Small larvae C. sonorensis ( C a m . ) Small larvae Netelia brevicornis ( C u s h m . ) L a r v a e / p u p a e

B r a c o n i d a e Apanteles marginiventris ( C r e s s . ) Small larvae Cardiochiles nigriceps ( V i e r . ) L a r g e l a r v a e Chelonus texanus ( C r e s s . ) E g g / l a r v a e Microplitis croceipes ( C r e s s . ) Small larvae

Trichogrammatidae Trichogramma s p p E g g s

D i p t e r a T a c h i n i d a e Archytas marmoratus ( T o w n s . ) Larvae/pupae Eucelatoria armigera ( C o q . ) L a r g e l a r v a e Lespesia aletiae( R i l . ) L a r g e l a r v a e Winthemia rufopicta ( B i g o t ) L a r g e l a r v a e o r l a r v a e / p u p a e

S o u r c e s : R i d g w a y a n d L i n g r e n ( 1 9 7 1 ) ; D a n k s e t a l . ( 1 9 7 9 ).

tion is being considered (R. Hill, personal insecticides in pilot field trials, but later gave inco n • communication). sistent results because it was inactivated by sun• light. Various attempts have been made to Pathogens overcome this problem, including mixing it with attractive baits, but the real breakthrough came B e c a u s e of the n e e d to r e d u c e the a m o u n t of w h e n the virus w a s incorporated into a c a p s u l e insecticide u s e d in Heliothis control, a great deal of with UV light screening agents, a n d n o w several work has been done on pathogens that affect boll- improved commercial formulations are available in worms, notably by CM. Ignoffo and his coworkers the USA. Ignoffo a n d C o u c h (1981) provide a c o m • ( s e e Ignoffo 1975). Bacillus thuringiensis Berliner prehensive review of the research leading to the works well in the laboratory, but impractically large development of NPV as a commercially available a m o u n t s h a v e b e e n n e e d e d t o give effective c o n • product. trol on cotton (Dulmage 1972). However, Gentry et Trials with NPV w e r e carried out on H. armigera al. (1969) achieved encouraging results against H. in U g a n d a (Coaker 1958) South Africa (Whitlock virescens on t o b a c c o in a 2-y ear integrated control 1977) a n d B o t s w a n a ( R o o m e a n d Daoust 1976) p r o g r a m , a n d there is every r e a s o n to believe that but have not b e e n followed up. B. thuringiensis will soon be a practical alternative In the USA, experiments are being carried out to to insecticides for Heliothis control. evaluate a microsporidian, Vairimorpha necatrix for T h e Heliothis nuclear polyhedrosis virus (NPV), control of lepidopterous pests, but in trials to date Baculovirus heliothis, is specific to Heliothis spp with Heliothis spp, it has been less effective than a n d is h a r m l e s s to m a n , d o m e s t i c a n d wild animals, chemicals, in spite of achieving high rates of infec• beneficial insects, and plants. It compared well with tion (Maddox et al. 1981).

1 5 3 Table 5. Primary parasitoids of Heliothis spp in Australian cotton fields.

S t a t e P a r a s i t o i d New South Wales Queens land

Hymenoptera Ichneumonidae Heteropelma scaposum ( M o r l e y ) + + Lissopimpla excelsa ( C o s t a ) + + Netelia producta ( B r u l l e ) + + Pterocormus promisorius ( E r i c h s . ) + +

B r a c o n i d a e Cardiochiles sp + - Microplitis sp + + Three undetermined spp + -

Trichogrammatidae Trichogramma sp + + Trichogrammatoidea sp - - Scelionidae Telenomus s p . + +

D i p t e r a T a c h i n i d a e Carcelia noctuae ( C u r r a n ) + + ChaetophthaImus ? biseriatus M a l i + + Two undetermined spp + +

Sources : Bishop and Blood (1977); Room (1979).

Discussion devised to minimize damage to them. There are also opportunities for enhancing their action by timed releases, as has been demonstrated with The predator complex attacking Heliothis s p p is Chrysopa carnea in the USA. A further possibility is similar in all areas to that found in the USA (Table 3) the discovery of pesticide-tolerant strains and their and consists principally of predatory Hemiptera, establishment in crops to replace pesticide- Chrysopa spp, Coccinellidae, and spiders. Thus, susceptible populations that have been eliminated. prospects for introduction of species from one Many of the parasitoids are specific to Heliothis region to another are poor and could be detrimental spp or are oligophagous—attacking a narrow in that they may turn their attention to beneficial range of related hosts. Because of their intimate species employed in biological control of other relationship with their hosts, these parasitoids are pests, including weeds. more reliable mortality factors, and their manipula • For example, in Mauritius, releases of the redu- tion is likely to have a greater impact than that of viid, Sycanus intagator Stal., from India were general predators. Comparison of the parasitoid stopped, because of concern that it would prey spectrum in different regions (Tables 1, 2, 4, 5) upon larvae of Schematiza cordiaei Barber (Chry- shows similarities both taxonomic and functional. somelidae), which had been successfully intro• In fact, some species are common to both Africa duced for control of a serious weed, Cordia a n d India. curassavica. On the other hand, general predators Very crudely, Table 6 compares the parasite are an important mortality factor to be conserved, spectra in different areas and suggests that there and pesticide application strategies should be are a limited number of available niches to be filled,

154 Table 6. Comparison of parasite spectra of Heliothis spp In different areas.

A r e a Heliothis s t a g e P a r a s i t e A f r i c a A u s t r a l i a I n d i a USA parasitized

Ichneumonidae Campoletis, Eriborus,Charops + + + + S m a l l l a r v a e Enicospilus, Netelia + + + + Large larvae

B r a c o n i d a e + Chelonus + - (-)a E g g / l a r v a e Apanteles. Microplitis + + (-)a + S m a l l l a r v a e Bracon + + Larvae external g r e g a r i o u s Cardiochiles + + - + Large larvae Trichogrammatidae Trichogramma. Trichogrammatoidea + + + + Eggs

Scelionidae a Telenomus + + - (-) Eggs

T a c h i n i d a e Palexorista, Carcelia, + + + + L a r v a e Eucelatoria, Lespesia A r c h y t a s . Winthemia + ? + + Larvae/pupae Goniophthalmus

a . Present but ineffective.

Some gaps appear to exist in some regions; nota• research, as most parasitoid groups are poorly bly, scelionids (Telenomus spp) are not recorded in understood and much confusion exists as to the India; Chelonus sp in India and Australia; Apanteles identity of common species. For example, recent spp in Australia, and Bracon spp in Australia and studies on Trichogrammatidae have shown that the USA. more species exist than had previously been real• These gaps offer the best opportunities for intro• ized, and that many of them can only confidently be duction of exotic species. It is also possible that isolated and characterized following careful exper• species from another continent may be inherently imentation with live material under standardized superior to native ones and so be able to displace conditions (Nagarkatti and Nagaraja 1977). them and raise overall mortality (DeBach 1966). A Bioecological studies are also essential to the third possibility is the introduction of strains of s p e • development of management strategies to con• cies, native or otherwise, that are pesticide- serve and enhance the action of indigenous para• tolerant. These prospects cannot be fully evaluated sitoids and predators. at present, as there are too few studies on regional Records of nematode parasites, usually Mermi- parasite complexes, and undoubtedly many useful thidae, are available from all regions where inven• parasitoids remain to be discovered. For example, tories of natural enemies are available. However, research currently under way in Bolivia is turning significant rates of parasitism are only achieved at up new species of egg parasitoids (F.D. Bennett, irregular intervals, when climatic conditions are personal communication). favorable, and it has so far not been possible to Further bioecological studies are also needed in overcome this limitation or to culture mermithids for areas where no recent surveys have been made to inundative release. Thus, for the time being, nema- enable reevaluation and detection of changes todes are not of practical value as biotic pest con- brought about by intensification of agriculture. trol agents. Such studies must be backed by sound taxonomic Pathogens are present in most Heliothis s p p

155 populations, but they are not reliable contro l sia. B e s i d e s c a r r y i n g out r e s e a r c h a n d information agents, e x c e p t w h e r e e p i d e m i c s c a n b e i n d u c e d , w o r k itself, t h e UK unit also maintains links with but as mortality rapidly falls to e n d e m i c levels, their collaborating institutes. In t h e past, the C I B C has use is principally as specific biological pesticides. m a d e studies on Heliothis s p p natural e n e m i e s at R e c e n t a d v a n c e s in t h e handling, culture, a n d its stations a n d is currently involved in providing a p p l i c a t i o n of p a t h o g e n s h a v e m a d e their use a parasitoid cultures for India a n d N e w Z e a l a n d . p r a c t i c a l reality a n d a valuable tool in pest m a n • T h e C I B C w o u l d be glad to take part in n e w a g e m e n t . H o w e v e r , relatively high cost, rapid d e t e • initiatives related to Heliothis s p p m a n a g e m e n t as rioration in s t o r a g e under tropical conditions, a n d s u g g e s t e d in this paper. ready inactivation by ultraviolet light limit their u s e • f u l n e s s at present. Conclusion

T h e f e w reported attempt s at biological control of The CIBC and Heliothis Heliothis s p p by introduction of natural e n e m i e s Management w e r e not s u c c e s s f u l . R e c e n t C I B C projects have i n c l u d e d t h e supply of parasites f r o m India for T h e C o m m o n w e a l t h Institute of Biological Control, release in Mauritius a n d of parasites f r o m Europe f o u n d e d in 1 9 2 7 , is a constituent of t h e C o m m o n • for release in N e w Z e a l a n d . T h e results of these are w e a l t h Agricultural B u r e a u x (CAB), a n international a w a i t e d with particular interest, as the c i r c u m s t a n • organization set up a n d f u n d e d by g o v e r n m e n t s of c e s are favorable; both release areas are islands t h e British C o m m o n w e a l t h countries, but its servi• a n d p r e s u m a b l y have predominantly, if not entirely, c e s are o p e n to all. T h e C I B C is b a c k e d by the C A B nonmigrant populations. In m o r e c o m p l e x c o n d i • Information a n d Identification Services a n d is tions on continents, the prospects for straightfor• d e v e l o p i n g a network of collaborating a g e n c i e s w a r d c l a s s i c a l biological control a p p e a r less t h r o u g h t h e unit set up in J u n e 1981 at Imperial promising. College, S i l w o o d Park, Ascot, in the UK. T h r o u g h • It s e e m s m o r e likely that in most areas, the aim out its e x i s t e n c e , the C I B C has built up expertise in must be integrated control, particularly on c r o p s t h e use of a r t h r o p o d parasitoids a n d predators in s u c h as c o t t o n , w h e r e Heliothis s p p are part of a a r t h r o p o d pest a n d w e e d control, chiefly related to diverse pest c o m p l e x . Bacillus thuringiensis a n d the introduction of natural e n e m i e s for " c l a s s i c a l " NPV s h o u l d provide treatments that will c o n s e r v e biological control. As well as undertaking research natural e n e m i e s w h e r e a r t h r o p o d natural e n e m i e s o n c o n t r a c t , the C I B C provides a d v i c e , information, are i n a d e q u a t e . H o w e v e r , t h e r e c e n t investigations a n d training. S i n c e 1975, it has b e g u n to actively o n the E u r o p e a n parasites, w h i c h a c h i e v e s u b • w i d e n its s e r v i c e with r e g a r d to t h e r a n g e of natural stantial rates of parasitism in spite of heavy insecti• e n e m i e s s t u d i e d a n d the w a y s i n w h i c h they are c i d e u s a g e on intensively cultivated land, suggest u s e d . Within its sister institutes in t h e C A B o r g a n i • the n e e d for a critical reappraisal. N e w studies zation, expertise is n o w available on insect n e m a - s h o u l d i n c l u d e e v a l u a t i o n of other parasite s p e c i e s tology a n d m y c o l o g y ; in addition, t a x o n o m i s t s a n d strains for their ability to maintain effective u n d e r t a k e identification of insects, helminths population densities in pesticide-polluted agroeco- (including n e m a t o d e s ) , fungi, a n d s o m e bacteria. In s y s t e m s . With the k n o w n differences in parasite a s s o c i a t i o n with Imperial College, t h e U K G l a s s - f a u n a a n d a b u n d a n c e in different c r o p s , particular h o u s e C r o p s R e s e a r c h Institute, a n d the UK Insti- attention s h o u l d be paid to studies in target c r o p s tute of Virology, the C I B C n o w provides a service a n d a s s o c i a t e d alternative host plants. including all a s p e c t s of a r t h r o p o d pathology, p o p u • A further n e e d is to d e t e r m i n e the extent of lation d y n a m i c s , a n d c o m p u t e r - a s s i s t e d analysis migration. If migration is significant, attention to the a n d m o d e l i n g . feasibility of periodic release of natural e n e m i e s will T h e C I B C h a s regional field stations in Trinidad, be n e c e s s a r y , unless natural e n e m i e s with similar Switzerland, K e n y a , India, a n d Pakistan, w h i c h pro• migration patterns c a n be located. Alternatively, if vide b a s e s for field studies a n d provide cultures of infestations chiefly derive f r o m b r e e d i n g in other natural e n e m i e s . W o r k i s also c a r r i e d out f r o m t e m • plants in s u r r o u n d i n g cultivated areas, a s e a r c h porary substations set up to u n d e r t a k e specific for natural e n e m i e s effective in t h e s e habitats will p r o j e c t s — c u r r e n t l y i n M e x i c o , G h a n a , a n d M a l a y - be indicated; s u p p r e s s i o n by alteration of the

1 5 6 surroundings to discourage Heliothis spp also CARL, K.P. 1977. Survey, propagation and importation becomes a possibility, as does the encouragement of natural enemies of Heliothis armigera Hb. Annual of plants supporting those natural enemies that report for 1976, Commonwealth Institute of Biological thrive within the crop. Control, Delemont, Switzerland. In each instance, detailed ecological studies are CARL, K.P. 1978. Heliothis armigera; parasite survey required to seek out means of exploiting natural and introduction of Apanteles kazak to New Zealand. enemies. A less thorough approach is unlikely to Report of work in 1977-78. Report, Commonwealth Insti• lead to effective biological or integrated control. As tute of Biological Control, Delemont, Switzerland.

Heliothis spp are of importance throughout sub• COAKER, T.H. 1958. Experiments with a virus disease tropical and tropical regions on several major of the cotton bollworm Heliothis armigera (Hbn.). Annals crops, a wide-ranging coordinated research pro• of Applied Biology 46: 536-541. gram is most likely to achieve progress. The net• COAKER, T.H. 1959. Investigations on Heliothis armig• work of regional stations operated by the CIBC era (Hb.) in Uganda. Bulletin of Entomological Research provides centers where such studies can be 50: 484-506. undertaken. Its UK unit and associated institutes DANKS, H.V., RABB, R.L., and SOUTHERN, P.S. can provide backup research and services on all 1979. Biology of insect parasites of Heliothis larvae in aspects of pest management, information retrieval, North Carolina. Journal of the Georgia Entomological and identification of arthropods and pathogens. Society 14(1): 36-64.

De BACH, P. 1966. The competitive displacement and co-existence principles. Annual Review of Entomology 11: 183-212. DOUTT, R.L., and SMITH, R.E. 1971. The pesticide References syndrome—diagnosis and suggested prophylaxis. In Bio• logical control (ed. C.B. Huffaker). New York, USA: Ple• ACHAN, P.O., MATHUR, K.C., DHARMADIKARI, num Press. 511 pp. P.R., and MANJUNATH, T.M. 1968. Parasites of Helio- this spp in India. Technical Bulletin of the Commonwealth DULMAGE, H.T. 1972. Pathogens. Pages 57-64 in Institute of Biological Control 10: 129-147. Southern Cooperative Series Bulletin 169, Oklahoma Agricultural Experiment Station, Oklahoma State Univer• BAR, D., GERLING, D., and ROSSLER, Y. 1979. Bio- sity, Stillwater, Okla, USA. nomics of the principal natural enemies attacking Helio• this armigera in cotton fields in Israel. Environmental GENTRY, C.R., THOMAS, W.W., and STANLEY, J.M. Entomology 8: 468-474. 1969. Integrated control as an improved means of reduc• ing populations of tobacco pests. Journal of Economic BENNETT, F.D., and YASEEN, M. 1972. Parasite intro• Entomology 62: 1274-1277. ductions for the biological control of three insect pests in the Lesser Antilles and British Honduras. PANS 18: 468- GREATHEAD, D.J. 1966. Memorandum on the paras• 474. ites and possibilities of biological control of East African boll worms, Commonwealth Institute of Biological Control, BHATNAGAR, VS. 1980. A report on research on the Kampala, Uganda. 21 pp. Heliothis complex at ICRISAT (India) 1974-1979. Pres• ented at the All India Workshop on Consolidation of Pest HARDWICK, D.F. 1965. The corn earworm complex. Management Recommendations and Guidelines of Memoirs of the Entomological Society of Canada 40: Research. 24-26 Apr 1980, Udaipur, India. 1 -247.

BISHOP, A.L., and BLOOD, P.R.B. 1977. A record of IGNOFFO, C.M. 1975. Entomopathogens as insecti• beneficial arthropods and insect diseases in southeast cides. In Insecticides of the future, ed. M. Jacobson. New Queensland cotton. PANS 23: 384-386. York, USA: Marcel Dekker. 93 pp.

BOGUSH, P.O. 1957. Parasites of the cotton bollworm, IGNOFFO, C.M., and COUCH, T.L. 1981. The nucleo- Chlorides obsoleta F., reared in Turkmenia. Entomolo- polyhedrosis virus of Heliothis species as a microbial gikekoe Obozrenie 36: 98-107. (In Russian.) insecticide. Pages 329-362 in Microbial control of pests and plant diseases 1970-80 (ed. H.D. Surges). London, BOWDEN, J. 1973. Migration of pests in the tropics. UK: Academic Press. Mededelingen Fakuteit Landbouwwetenschappen, LINCOLN, C. 1972. Distribution, abundance and control Ghent 38: 785-796. of Heliothis spp. in cotton and other host plants. Pages 2-7 CAMPBELL, B.C., and DUFFEY, S.S. 1979. Tomatine in Southern Cooperative Series Bulletin 169, Oklahoma and parasitic wasps: potential incompatibility of plant anti• Agricultural Experiment Station, Oklahoma State Univer• biosis with biological control. Science 205: 700-702. sity, Stillwater, Okla, USA.

157 MADDOX, J.V., BROOKS, W.W., and FUXA, J.R. 1981. in soils in Botswana. Journal of Invertebrate Pathology Vairimorpha necatrix, a pathogen of agricultural pests: 27:7-12. potential for pest control. Pages 587-594 in Microbial WHITLOCK, V.H. 1977. Simultaneous treatments of control of pests and plant diseases 1970-1980, ed. H.D. Heliothis armigera with a nuclear polyhedrosis and a Burges. London, UK: Academic Press. granulosis virus. Journal of Invertebrate Pathology MANJUNATH. T.M. 1972. Biological studies on Tricho- 29:297-303. grammatoidea armigera Nagaraja, a new dimorphic egg parasite of Heliothis armigera (Hubner) in India. Entomo- phaga 17:131-147.

NAGARKATTI, S., and NAGARAJA, H. 1977. Biosys- tematics of Trichogramma and Trichogrammatoidea species. Annual Review of Entomology 22:157-176.

NETTLES, W.C. 1979. Eucelatoria sp. females: factors influencing response to cotton and okra plants. Environ• mental Entomology 8:619-623.

NEWSOM, L.D. 1972. Theory of population manage• ment for Heliothis spp. in cotton. Pages 80-92 in Okla• homa Agricultural Experiment Station, Oklahoma State University, Stillwater, Okla, USA.

PARSONS, F.S. 1940. Investigations on the cotton bollworm Heliothis armigera Hubn. (obsoleta Fabr.) Part II. The incidence of parasites in quantitative relation to bollworm populations in South Africa. Bulletin of Entomologi• cal Research 31.89-109.

PLAPP, F.W., and VINSON, S.B. 1977. Comparative toxicities of some insecticides to the tobacco budworm and its ichneumonid parasite, Campoletis sonorensis. Environmental Entomology 6:381 -384.

RAO, V.P. 1968. Heliothis spp. and their parasites in India. PANS (A) 14:367-375.

REED, W. 1965. Heliothis armigera (Hb.) (Noctuidae) in Western Tanganyika II. Ecology and natural and chemical control. Bulletin of Entomological Research 56:127-140.

RIDGWAY, R.L., and JONES, S.L. 1969. Inundative releases of Chrysopa carnea for control of Heliothis on cotton. Journal of Economic Entomology 62:177-180.

RIDGWAY, R.L., and LINGREN, P.D. 1972. Predace- ous and parasitic arthropods as regulators of Heliothis populations. Pages 48-56 in Southern Cooperative Series Bulletin 169, Oklahoma Agricultural Experiment Station, Oklahoma State University, Stillwater, Okla, USA.

ROBINSON, B.R., YOUNG, J.H., and MORRISON, R.D. 1971. Strip-cropping effects on abundance of Heli- othis damaged cotton squares, boll placement, total bolls and yields in Oklahoma. Environmental Entomology 1: 140-145.

ROOM, P.M. 1979. Parasites and predators of Heliothis spp. (Lepidoptera: Noctuidae) in cotton in the Namoi Vel- ley, New South Wales. Journal of the Australian Entomo• logical Society 18:223-228.

ROOME, R.E.,and DAOUST, R.A. 1976. Survival of the nuclear polyhedrosis virus of Heliothis armigera on crops

158 The Utilization of Biological Control in Heliothis Management in India

Sudha Nagarkatti*

Abstract Heliothis armigera causes extensive losses to food and fiber crops in India. Indiscriminate pesticide use and the availability of monocultures of preferred host plants have aggravated the problem. In the last 2 or 3 years, efforts have been in progress to make inundative re• leases of exotic parasites and to utilize indigenous nuclear polyhedrosis virus against H. armigera. The use of egg parasites such as Trichogramma spp appears promising, but inun• dative releases ot egg-larval and larval parasites have limited scope because of difficulties in mass rearing. The regulatory action ot predators is poorly understood, but their conserva• tion could be considered. Amongst recent introductions are Eucelatoria bryani (Coq.) and Apanteles marginiventris (Cresson), but only the former has been released and recovered in the field. Consideration should be given to importation of parasites such as Telenomus sp nr triptus Nixon from Australia, Hyposoter didymator Thbs. and Apanteles kazak Telenga -which show insecticide tolerance-from Europe, and several tachinid parasites from the neotropics that appear to be suitable candidates lor introduction. Amongst pathogens there is scope lor utilizing the indigenous nuclear polyhedrosis virus. The role of weeds in influencing natural enemy populations needs to be studied, and insecticides with selective action and greater safety to natural enemies need to be identi• fied. In order to achieve biological control, several nonchemical approaches would have to be combined. Greater emphasis on exotic natural enemy introduction will require interna• tional cooperation, while a good surveillance and forecasting system will enable implementa• tion of appropriate control measures in areas where migrations are imminent.

T h e n o c t u i d Heliothis armigera (Hb) as a pest of an This a n d related species s u c h as H. zea (Boddie), extensive range of cultivated c r o p s has no equal. H. virescens Fab., H. punctigera Wall., etc., have

*National Centre for Biological Control lndian lnstitute of Horticultural Research (ICAR), Bangalore, India

Contribution No.2/82 of the Indian Institute of Horticultural Research. Bangalore, India.

International Crops Research Institute for the Semi-Arid Tropics. 1982 Proceedings of the International Workshop on Heliothis Management 15-20 November 1981, Patancheru, A.P., India 159 probably drawn the attention of more economic are well-timed and adequate numbers released at entomologists than any other pest. In India, H. frequent intervals. Ridgway et al. (1974) recom• armigera is a limiting factor in pulse production, mend 100 000 Trichogramma per acre (247 often causing total crop loss. Seshu Reddy and 000/ha) at 2- or 3-day intervals, but earlier reports Channa Basavanna (1978) estimated that an aver• (Goretzkaya 1940) indicate that in Azerbaidjan, age infestation of one larva per plant of pigeonpea releases of 200 000 per acre (494 000/ha) in five can cause a yield loss of 1015 kg/ha. In sorghum, batches of about 40 000 each at intervals of 3 days yield losses of 18 to 26% have been reported gave parasitism of 40 to 80% throughout the period (Rawat et al. 1970), while in cotton in Madhya Pra• of application. Bournier and Peyrelongue (1973) desh, losses of 41 to 56% occur (Kaushik et al. also reported that in Madagascar preflowering 1969). In horticultural crops such as tomato, yield releases of T. brasiliensis Ashm. appeared very losses of 40 to 50% are reported in Tamil Nadu promising. (Srinivasan 1959). Amongst Trichogrammatidae, those most com• The problem has apparently been aggravated, monly reared from Heliothis eggs in India are T. as with many other pests, by indiscriminate pestici- chilonis Ishii, T. chilotraeae Nagaraja and Nagar- dal applications, including aerial spraying in some katti, a n d Trichogrammatoidea armigera M a n j u - areas like Gujarat, which has adversely affected nath. In Gujarat, Manjunath et al. (1976) found that the natural enemy populations. Contributing fac• T. chilotraeae was abundant on H. peltigera tors in India include the continuous availability of (Schiff.) eggs laid on the weed starburr (Acanthos- monocultures of cotton, pigeonpea, chickpea, permum hispidum). lucerne, maize, sorghum, potato, groundnut, etc., T h e use of Trichogramma spp has certain limita• and the lack of crop rotation, which would break the tions, besides the fact that they have poor search• Heliothis c y c l e . ing ability, which necessitates the release of Because of the high cost of protecting crops massive numbers. Studies on natural parasitism f r o m Heliothis spp with chemical pesticides and the have shown that adult Trichogramma avoid crops increasing concern over residues in food, there is such as pigeonpea and chickpea. Bhatnagar and growing interest in the use of natural enemies for Davies (1978) found that while egg parasitism was controlling these pests. The prospects of using as high as 80% on sorghum and cowpea, it was classical biological control, involving introduction negligible on pigeonpea and chickpea, which suf• of exotic natural enemies are not considered to be fered heavy damage by larvae of H. armigera. This bright (Anonymous 1978), in view of the migratory is attributed to the glandular hairs on the leaves, behavior of moths and the sudden influx of popula• which produce an acidic exudate. However, there tions to which resident natural enemies may not be is scope for using Trichogramma spp in such crops able to respond readily. In India, it is only in the last as cotton, sorghum, maize, sunflower, and ground- 2 or 3 years that efforts have been in progress to nut, where such a problem does not exist. see if exotic natural enemies can be utilized. During the 1980-81 cotton season in Gujarat, This paper is not intended to be a review of extremely encouraging results have been obtained biological control efforts against Heliothis s p p in from releases of T. brasiliensis a n d T. achaeae N. India and elsewhere. Rather, an attempt has been and N., in addition to larval parasites of bollworms, made to see how best the available information in an insecticide-free 2-ha plot at Karvan (Baroda could be utilized to enhance the regulatory action district) by the Gujarat Agricultural University under of natural enemies, particularly of H. armigera, the All India Coordinated Research Project on Bio• which is the dominant pest species of the Heliothis logical Control. Yields were found to be compara• complex in this country. ble to those in pesticide-treated plots (Anonymous 1981), but confirmation of results in the current Inundative Releases of Indigenous season is awaited. Parasites and Predators Egg-Larval and Larval Parasites Egg Parasites Hymenoptera Utilization of egg parasites such as Trichogramma spp should be considered seriously, since damage While efforts have been made by various workers to the crop can be greatly reduced if the releases to study the biology of hymenopterous and dipter-

160 ous parasites and develop mass-rearing tech• mon in cotton fields in India, no effort has been niques (Tikar and Thakare 1961; Gangrade 1964; made hitherto to breed them for inundative release. Achan et al. 1968; Patel et al. 1970; Patel and Singh A method for mass-rearing C. scelestes has s i n c e 1972; Patel et al. 1973), the egg-larval parasite been developed (Krishnamoorthy and Nagarkatti, Chelonus heliopae Gupta and larval parasites, in press) based on the technique described by s u c h as Campoletis chlorideae Uchida and Eribo- Ridgway et al. (1970), except that frozen eggs of rus spp are not amenable to mass-rearing, and the Corcyra cephalonica St. are used instead of Sito- process is not economical. A problem with sex ratio troga cerealella (Oliv.). At present, inundative favoring males is a major impediment in laboratory releases of C. scelestes are in progress in cotton in cultures. In some countries, particularly the USSR, Gujarat, although the numbers being released are use of larval parasites such as Bracon brevicomis not as high as recommended by Ridgway et al. (Wesm.) at the rate of 10 000 per hectare in cotton (1970). The results of these releases will be known has been recommended (Skoblo 1940), but despite only after harvest is completed and yield data the ease of rearing this parasite, it has not been become available. tried so far against H. armigera in India. Predators such as nabids, pentatomids, and reduviids are known, e.g., Sycanus indagator Stal., Diptera Rhinocoris fuscipennis F., R. marginatus F.,Andral- lus spinidens (Fabr.), etc., but may not show signifi- Amongst the indigenous Diptera, breeding of cant impact on Heliothis populations because they Palexorista laxa (Curran) [= Drino munda (Wied.)] are general predators and are not likely to concen• is relatively easy and has been standardized by trate on Heliothis eggs or larvae as prey. At best, entomologists in the USA (Chauthani and Hamm conservation of these general predators can be 1967), where it was introduced. However, no efforts considered. have been made to undertake inundative releases of these species in India to my knowledge, but may be worth considering. Rearing methods for Carce- Importation of Exotic lia ( = Senometopia) illota (Curran) have been deve- Natural Enemies loped (Patel et al. 1970). Goniophthalmus halli Mesn., a microtype egg-laying species, can also be Classical biological control, involving importation mass-bred (Patel and Singh 1972). For G. halli, a of exotic natural enemies, has not been tried in technique similar to that developed for the sugar- India except in a limited way, and only in the last 2 cane borer parasite Palpozenillia palpalis (Ald.) by or 3 years. The Commonwealth Institute of Biologi• Simmonds (1958) can be utilized, but both are cal Control, Indian Station, first imported the labor-intensive and would not be suitable for con- tachinid Eucelatoria bryani (Coq.) (earlier called E. sideration in any inundative release program where armigera) from the USA in 1978 and found that it economy of production has to be kept in mind. successfully parasitized H. armigera. The tachinid Peribaea orbata (Wied.), can also Subsequently, Pawar et al. (1981) reported that be mass-bred easily in the laboratory and being from January 1979 to April 1980, a total of 1560 gregarious, yields of puparia are substantial. This mated females of E. bryani were released in tomato species is not specific to Heliothis, being also para• fields around Bangalore, along with 798 larvae par• sitic on Spodoptera spp, and hence its impact on H. asitized by the dipteran. The authors also reported armigera is likely to be dissipated. that recoveries were made on four occasions. The In general, however, the mass-rearing of larval same parasite was also bred at the National Centre parasites of H. armigera, particularly those that are for Biological Control, Bangalore, and 435 mated solitary, is laborious and uneconomical, since the females released in a tomato crop near Hessa- parasitized larvae have to be reared in isolation to raghatta, 26 km from Bangalore. Sporadic recover• avoid cannibalism. This makes the use of larval ies indicate that the parasite is adaptable to the parasites for inundative release an unattractive climatic conditions around Bangalore and could proposition. possibly become a permanent component of the parasite complex. It is not known how the parasite Predators will perform in relation to indigenous dipterous par• asites and whether the fact that it is gregarious will Although it is well known that Chrysopa spp, e.g., C. give it any marked advantage over some of the carnea Steph., C. scelestes Banks, etc., are com-

161 indigenous species. Releases of E. bryani w e r e H. gelotopoeon (Dyar); Actinophaga koehleri also made in pigeonpea and chickpea at Patan- Blanch., which has been recorded only from Helio• cheru, near Hyderabad, giving 14.2% and 4% par• this spp; a n d Lespesia aletiae (Riley) which has asitism respectively in field-cage studies been recorded from H. zea, H. virescens, etc., are (Sithanantham and Reed 1980). The next few years some of the tachinids that may prove useful. will show how effective the parasite is proving. At a recent workshop on biological control of At the National Centre for Biological Control, we Heliothis spp held in Australia (Twine 1980) a have recently obtained a culture of Apanteles mar- number of papers were presented that include lists giniventris (Cresson) from the USA, where it of natural enemies and details of their effective• attacks a wide range of Noctuidae, including Helio- ness in Australia and Africa. This compilation coul d this spp. Preliminary studies have shown that it be very useful in selecting candidate species for a c c e p t s H. armigera as well as Spodoptera litura trials in India. (F.). If the crop stature has any influence on the activity of the Diptera—as is indicated by reports of Bhatnagar and Davies (1977a), who found that Use of Bacterial and parasitism on chickpea by Diptera never exceeded Viral Pathogens 4.4%—there is reason to believe that E. bryani may not perform well in chickpea, but may prove better Although the bacterium Bacillus thuringiensis Ber• in crops such as cotton, tomato, and pigeonpea. liner is known to occur naturally in the field and has The performance of A. marginiventris in the field, been isolated from a number of lepidopterous particularly on crops like pigeonpea and chickpea, hosts, including H. armigera in India, its use on field will have to be determined and more emphasis scale has been strongly opposed by the silk indus• placed on importation of hymenopterous larval par• try. Despite assurances that the pathogen is widely asites for use on these crops. used in other countries—Japan and China, for Since egg parasitism by Telenomus spp on Heli- instance—where silk forms an important industry, it othis in India has not been observed, importation of is unlikely that the attitude of the concerned author• T. sp. nr. triptus Nixon from Australia, where it is ities, particularly in some of the states, will cha n g e . reported to give as much as 92.7% parasitism of Even if this were to happen, it will be a long time Heliothis spp (Twine 1973), must be considered. Its before commercial production of an acceptable effectiveness in crops that are avoided by Tricho- formulation is started. Meanwhile, it is necessary to gramma spp would have to be studied. screen strains of B. thuringiensis that are less toxic We propose to introduce several other exotic to silkworms and could be profitably used in parasites of Heliothis over the next few years. If a agriculture. good balance is to be struck between parasite and The occurrence of nuclear polyhedrosis virus insecticide use, it would be desirable to test spe• (NPV) in H. armigera was reported from India by cies that are relatively tolerant to insecticides. T h e Patel et al. as early as 1968. Although the disease is European parasites Hyposoter didymator T h b s . widely prevalent in laboratory cultures, natural inci• a n d Apanteles kazak Telenga, which give high dence in the field has rarely been observed. Rabin- rates of parasitism even in heavily sprayed areas, dra and Subramaniam (1973) also reported the may be suitable for use in integrated control pro• presence of a cytoplasmic polyhedrosis virus grams and must be given preference. A. kazak also (CPV) in laboratory cultures of H. armigera. M o r e has the advantage of a short life-cycle (10-18 recently, cultures of the insect maintained at our days), which compares favorably with that of H. Centre have revealed the presence of a granulosis armigera. virus. Sabrosky (1978) has listed a number of tachinid Though the use of the NPV in cotton in Uganda parasites of Heliothis spp from the western hemis• (Coaker 1958) and Botswana (Roome 1971) has phere. Amongst these, those species that show not been considered to be very effective, in India greater affinity for Heliothis than for other noctuids Narayanan (1980) described field studies on the must certainly be considered for trials, since NPV in chickpea. He states that application of the tachinids are powerful fliers and could conceivably virus at 250 and 125 larval equivalents per ha dur• migrate along with the pest. Three species of ing evening hours thrice at weekly intervals after l n c a m y i a — l . charlini Cortes, /. chilensis Ald. and /. appearance of young larvae caused significant spinicosta Ald.—which have been recorded from reduction in infestation, treated plants showing

162 5.15 a n d 7.85 larvae per 10 plants, respectively, as effectively suppresses H. armigera populations on against 27.65 in untreated controls. Moreover, cotton a n d c h i c k p e a in the USSR. S u c h studies virus-treated plots c o m p a r e d favorably with t h o s e have apparently not b e e n m a d e in India in relation treated with 0.07% endosulfan. to Heliothis. No efforts have b e e n m a d e t h u s far to utilize In addition to eradication of the weeds, another c o m m e r c i a l preparations of Baculovirus heliothis, avenue of r e s e a r c h that probably warrants effort, is s u c h as Elcar, that are already available in other control of H. armigera in w e e d stands, either by countries, or to p r o d u c e the indigenous virus on a inundative releases of parasites s u c h as Tricho- c o m m e r c i a l scale. T h e involved registration p r o c e • gramma w h e r e H. armigera abounds in the off- dures, etc., w o u l d deter local firms f r o m taking up season, or by treatment with appropriate c h e m i c a l s c o m m e r c i a l production. However, it s e e m s likely that will r e d u c e the pest population before the that farmers w o u l d consider the use of c r u d e s u s • major susceptible c r o p s are s o w n . pensions of viral material w h i c h they t h e m s e l v e s c a n prepare, as in the c a s e of S. litura. (In cotton, both in T a m i l N a d u a n d Gujarat, farmers have r e a d • Selective Use of Insecticides ily t a k e n to the preparation a n d use of the NPV). At T h e use of s o m e insecticidal applications m a y be our Centre we have n o w p r o d u c e d sufficient NPV unavoidable, considering the increased d e m a n d material to enable reasonably large-scale field for pulses, cotton, oilseeds, a n d cereals in the trials. We n o w p r o p o s e to undertake trials on differ• country, but the insecticides to be used should be ent c r o p s a n d standardize the treatment s c h e • selected with c a r e so that they do minimal h a r m to dules, s i n c e these c o u l d vary from c r o p to crop. predators a n d parasites. S u k h o r u c h e n k o et al. Lyophilization a n d preparation of formulated m a t e • (1977) have reported that phosalone is harmless to rial, w h i c h will facilitate field trials, is also being natural e n e m i e s a n d is therefore suitable for use in undertaken. T h e s c o p e of m i c r o e n c a p s u l a t i o n a n d integrated control programs. Endosulfan is fre• use of suitable indigenously available protectants quently c o n s i d e r e d to be safe to natural e n e m i e s to prevent inactivation of the virus polyhedra by UV on the basis of its relative safety to honeybees, but radiation is yet to be explored. our studies have indicated that this needs careful reappraisal, s i n c e the usually r e c o m m e n d e d d o s • ages have b e e n found highly toxic to s o m e of the The Role of Weeds in Heliothis parasites under rearing in our laboratory. It is Management obvious that insecticides such as D D T have a pro• n o u n c e d effect on parasitism levels, whatever the Bhatnagar a n d Davies (1977b) have reported that c r o p may be; Bhatnagar a n d Davies (1977), H. armigera has b e e n r e c o r d e d on 50 cultivated reported that in areas of A n d h r a Pradesh, parasit• plant s p e c i e s a n d 51 w e e d species. T h e y state that ism was as low as 1 to 3% in intercropped p i g e o n - the most significant carryover hosts in the hot pea sprayed with D D T as against 2 2 % in o n e s u m m e r are Datura metel, Acanlhospermum hispi- u n s p r a y e d field. Although it is r e c o m m e n d e d time dum, a n d Gynandropis gynandra. T h e r e is, h o w - a n d again that use of s u c h b r o a d - s p e c t r u m a n d ever, little information on the extent of parasitism of persistent insecticides in agriculture should be dis• H. armigera present on these w e e d s , a n d so it is c o u r a g e d , farmers continue to use them. Extensive difficult to a s s e s s to what extent the w e e d s help in s c r e e n i n g of insecticides readily available in India serving as reservoirs of the parasites or, alterna• should be undertaken with the objective of utilizing tively, to w h a t extent they are detrimental in serving only those that have a demonstrably higher degree as reservoirs of the pest itself. M o r e information of of safety to natural enemies. Unless this is d o n e the kind provided by M a n j u n a t h et al. (1976) w o u l d a n d r e c o m m e n d a t i o n s of insecticidal applications be required to m a k e a proper a s s e s s m e n t of the are b a s e d on s u c h studies, it w o u l d be meaningless role of w e e d s . t o c o n s i d e r a u g m e n t i n g n a t u r a l e n e m y populations. T h e r e is s o m e e v i d e n c e in other countries that the elimination of w e e d s c a n help to r e d u c e Helio- this infestation in cultivated crops. For e x a m p l e , Discussion Lozina-Lozinskii (1954) has stated that destruction of Dafura s f r a e m o n i u m , H y o s c y a m u s niger, Abu- In view of the large n u m b e r s of host plants involved, tilon avicennae, a n d Solatium nigrum in the spring the o c c u r r e n c e of H. armigera throughout the y e a r

163 on cultivated crops and weed hosts, its migratory introduced parasite would have the best chance of behavior, etc., there is little doubt that the mana g e • establishing an adequate breeding stock in the new ment of this pest necessitates a judicious combina• environment and of further propagation. tion of biological control agents, insecticides, an d It is generally believed that control of pests by cultural practices. All nonchemical approaches introduced natural enemies is best achieved in would have to be considered, such as: habitats of intermediate stability, such as orchard 1. Conservation of existing natural enemies habitats, or of even greater stability such as forest by judicious use of chemicals and enhancing habitats (Hall et al. 1980). With a polyphagous pest their regulatory action by suitable modifica• like H. armigera, which in India occurs on one crop tion of the environment, e.g., by providing or another all through the year, the habitats in wh i c h nesting sites for vespids, kairomones for it survives can hardly be called temporary agroec- increasing efficiency of Trichogramma spp, osystems, although the crops are short-term ones nectar-bearing flowering plants to provide and periodical disturbances occur. food for adult parasites, etc. Concerted efforts would have to be made to 2. Screening for and use of resistant varie• obtain exotic parasites to suit each crop situation, ties of the crop plants—the feasibility of and unless a team is specially assigned for foreign which is already being studied in pigeonpea exploration, the process of obtaining parasite and chickpea by ICRISAT entomologists material would remain slow. (Reed et al. 1980). If inundative releases of parasites are to be done 3. Adoption of crop rotation and field sanita• on a countrywide scale, particularly in crops such tion, which will exclude the availability of suit• as cotton and pulses, the need for commercial- able host plants in quick succession. scale production of parasites will have to be ful• 4. Use of pheromone baits and light traps, filled. In the East European countries, particularly both as monitoring devices and control the USSR, large numbers of state-run insectaries m e a s u r e s . cater to the needs of farmers, while in the USA and 5. Use of biocontrol agents such as egg and UK private entrepreneurs operate efficient com• larval parasites and the nuclear polyhedrosis mercial insectaries. In India, only a few state-run virus, the latter in the manner of an insecti• parasite-breeding laboratories exist where T. chilo- cide when outbreaks of the pest are to be nis Ishii and parasites of Nephantis serinopa Meyr. reckoned with. are mass-bred for use in sugarcane and coconut, and even these units are unable to meet the 6. Adjustment of planting times, which will demand fully. help crops to escape oviposition by migrat• ing moths. Estimates of numbers needed per hectare (in other words "dosages") have yet to be worked out Introduction of exotic parasites should be consi• for various crops and pest population levels, but dered as a long-range plan, and releases of any information already available in the literature cou l d species under trial should not be abandoned pre• provide guidelines. maturely and before sufficient numbers are H. armigera can survive and develop over a wide released, as this could lead to wrong conclusions. range of temperatures. Eggs can develop from 14 In his review of natural enemy introductions into to 38°C, larvae from 14 to 36°C, and pupae from 11 Canada, Beirne (1975) has stressed the impor• to 34°C (Rubtzov 1941). This would indicate that tance of numbers released. He estimated that of unless the parasites can also tolerate and develop the species released in totals of under 5000, only under these conditions, they would not be able to 10% became established; of the 5000 to 31 200 give satisfactory control of the pest. Hence, if the group, 40%; but of the over 31 200 group, as many parasite is to be mass-bred for field release, it as 78%. He therefore concluded that the greater would be necessary to simulate field conditions to the number released, the greater the likelihood of the maximum extent possible. If, on the other hand, successful colonization, and that if the numbers an exotic parasite is being sought for inoculative were below some minimum (about 5000 individu• releases, it must be ensured that it originates fro m als), the probability of success was small. The an area with a climate similar to that of the area importance of the size of the founder population where it is to be introduced. and its genetic makeup can hardly be overem• Forecasting systems are as yet poorly deve• phasized. A large heterozygous population of the loped in India, and the need for these, particularly

164 with a pest like H. armigera, cannot be underesti• B E I R N E , B.P. 1975. Biological control attempts by intro• mated. Studies on population dynamics, both of the d u c t i o n s against pest i n s e c t s in the field in C a n a d a . C a n • pest and of its natural enemies, need to be done a d i a n Entomologist 107 ( 3 ) 2 2 5 - 2 3 6 . over large plots (since small plots do not seem to B H A T N A G A R , V . S . , and D A V I E S , J . C . 1977a. Parasit• attract the pest) in different parts of the country, a n d ism levels on Heliothis armigera ( H u b n e r ) in s o m e this would require organized teamwork. If, in the pigeonpea and chickpea fields of farmers (1976-77). meantime, the breeding grounds are identified and C r o p p i n g E n t o m o l o g y Report 1 9 7 7 , I C R I S A T , P a t a n - migratory patterns properly established, the feasi• c h e r u , A.P., India. bility of making inundative parasite releases—both B H A T N A G A R , V . S . , and D A V I E S , J . C . 1977b. C r o p • in the locations where the buildup of the pest popu• p i n g e n t o m o l o g y , A n n u a l Report, 1 9 7 6 - 7 7 , I C R I S A T , lation is occurring and in the areas to which mass P a t a n c h e r u , A.P., India. migrations are likely to occur—can be planned in B H A T N A G A R , V . S . , and D A V I E S , J . C . 1978. C r o p p i n g advance and, conceivably, pest suppression entomology, progress report, 1977-78. ICRISAT, Patan• achieved. These releases may also have to be c h e r u , A.P., India. 30 p p . planned according to the phenology of the crops. In such situations, prophylactic sprays of the NPV or B O U R N I E R , J . P . , a n d P E Y R E L O N G U E , J . Y . 1973. Introduction, rearing a n d r e l e a s e s of Tricho- inundative releases of Trichogramma may be gramma brasiliensis A s h m . ( H y m . C h a l c i d a e ) w i t h a v i e w given priority. to c o n t r o l l i n g Heliothis armigera (Hbn.) (Lep. Noctuidae) It is evident from the foregoing discussion that in Madagascar Coton et Fibres Tropicales 28(2):231- the biological control of H. armigera populations 2 3 7 . requires cooperation at the national as well as at C H A U T H A N I , A B D U L , R., and H A M M , J . J . 1967. Biol- the international levels. Within the country, a o g y of t h e e x o t i c parasite Drino munda (Diptera: T a c h i n i - nationwide surveillance and forecasting system dae). Annals of the Entomological Society of America would help to alert entomologists in appropriate 60(4):373-376. areas of prospective migrations, while international C O A K E R , T . H . 1958. Experiments with a virus disease cooperation would greatly facilitate exchange of of t h e c o t t o n b o l l w o r m Heliothis armigera (Hbn.). A n n a l s promising natural enemies. of Applied Biology 46(4):536-541.

E H L E R , L.E., and M I L L E R , C . E . 1978. Biological con• Acknowledgments trol in temporary agroecosystems. Entomophaga 23:207- 2 1 2 .

The author is grateful to Dr. T. Sankaran, Principal G A N G R A D E , G . A . 1964. On the biology of Campoletis Entomologist and Entomologist-in-charge, Indian perdistinctus (Hymenoptera: Ichneumonidae) in Madhya Pradesh, India. Annals of the Entomological Society of Station, Commonwealth Institute of Biological Con• America 57(5):570-574. trol, Bangalore, for critically reviewing the manu• script and to Mr. M. Mani, Scientist S-1, Indian G O R E T Z K A Y A , I.N. 1940. T h e results o f the u s e o f t h e Institute of Horticultural Research, Bangalore, for Trichogramma of the A z e r b a i d j a n r a c e as a control m e a • assistance in reviewing literature. s u r e against t h e A m e r i c a n c o t t o n b o l l w o r m o n c o t t o n plants in A z e r b a i d j a n . S.S.R. Bulletin of Plant P r o t e c t i o n 1-2: 1 6 6 - 1 7 2 .

H A L L , R.W., E H L E R , L.E., a n d B I S A B R I - E R S H A D I , B . References 1980. Rate of success in classical biological control of arthropods. Bulletin of the Entomological Society of A C H A N , P.O., M A T H U R , K.C., D H A R M A D H I K A R I , America 26(2):111-114. P.R., a n d M A N J U N A T H , T . M . 1 9 6 8 . Parasites of H e l i o - this s p p . in India. T e c h n i c a l Bulletin of t h e C o m m o n w e a l t h K A U S H I K , U.K., R A T H O R E , V . S . , S O O D , N . K . Institute of Biological Control 10:129-149. 1 9 6 9 . I n c i d e n c e o f b o l l w o r m s a n d l o s s e s c a u s e d t o c o t • t o n i n M a d h y a P r a d e s h . I n d i a n J o u r n a l o f E n t o m o l o g y A N O N Y M O U S . 1978. Possibilities of biological control 31(2): 1 7 5 - 1 7 7 . of Heliothis armigera a n d H. zea. Commonwealth Institute of B i o l o g i c a l C o n t r o l status p a p e r 13, S l o u g h , U.K. 5 p p . KRISHNA MOORTHY, A., and NAGARKATTI, S U D H A . 1982. A m a s s - r e a r i n g t e c h n i q u e for Chrysopa A N O N Y M O U S . 1 9 8 1 . Annual report of work under All scelestes Banks (Neuroptera. Chrysopidae). Journal of India C o o r d i n a t e d R e s e a r c h Project o n B i o l o g i c a l C o n t r o l Entomological Research (In press.) o f C r o p P e s t s a n d W e e d s c a r r i e d out a t G u j a r a t A g r i c u l t u • ral U n i v e r s i t y , A n a n d , 1 9 8 0 - 8 1 . 3 1 p p . L O Z I N A - L O Z I N S K I I , L.K. 1954. T h e role of nutrition in

1 6 5 t h e d e v e l o p m e n t a n d r e p r o d u c t i o n o f t h e c o t t o n n o c t u i d R I D G W A Y , R.L., K I N Z E R , R.E., a n d M O R R I S O N , R.K. (Chloridea obsoleta Fabr.) Trudy vsesoyuznogo entomo- 1 9 7 4 . Production and supplemental releases of paras• l o g i c h e s k o g o o b s h c h e s t o v a , M o s k v a 4 4 : 3 - 6 1 . ites and predators for control of insect and spider mite p e s t s o f c r o p s . P a g e s 1 1 0 - 1 1 6 i n P r o c e e d i n g s , S u m m e r M A N J U N A T H , T . M . , P A T E L , R . C . , a n d Y A D A V , D . N . Institute of B i o l o g i c a l C o n t r o l of Plant I n s e c t s a n d D i s • 1 9 7 6 . Observations in Heliothis peltigera (Schiff.) (Lep., e a s e s (eds. F.G. M a x w e l l a n d F.A. Harris). J a c k s o n , M i s s , Noctuidae) and its natural enemies in Anand (Gujarat USA: University Press. State, India). P r o c e e d i n g s , I n d i a n A c a d e m y o f S c i e n c e s 8 3 ( B ) ( 2 ) : 5 5 - 6 5 . R I D G W A Y , R.L., M O R R I S O N , R.K., a n d B A D G L E Y , M . 1 9 7 0 . M a s s r e a r i n g a g r e e n l a c e w i n g . J o u r n a l o f E c o • N A R A Y A N A N , K. 1 9 8 0 . Field e v a l u a t i o n of a n u c l e a r nomic Entomology 63: 834-836. polyhedrosis virus of Heliothis armigera ( H u b n . ) on c h i c k - p e a , Cicer arietinum L. In P r o c e e d i n g s , W o r k s h o p on R O O M E , R . E . 1 9 7 1 . A n o t e o n t h e u s e o f b i o l o g i c a l Biological Control of Heliothis spp., D e p a r t m e n t of P r i m - i n s e c t i c i d e a g a i n s t H. armigera (Hb.) in B o t s w a n a . In ary I n d u s t r i e s , 2 3 - 2 5 S e p t 1 9 8 0 , T o o w o o m b a , Q u e e n s - Proceedings, Cotton Insect Control Conference, 24-27 l a n d , A u s t r a l i a . M a r c h 1 9 7 1 , B l a n t y r e , M a l a w i . 2 8 7 pp.

P A T E L , R . C . , P A T E L , J . C . , a n d P A T E L , J . K . N e w R U B T Z O V , I.A. 1 9 4 1 . Effect o f t e m p e r a t u r e a n d h u m i d • records of parasites of H. armigera (Hbn.) and H. peltigera ity on t h e d e v e l o p m e n t of e g g s a n d t h e l a r v a e of t h e boll (Schiff.) from Gujarat. Indian Journal of Entomology 3 3 ( 2 ) : w o r m . Bulletin o f Plant P r o t e c t i o n , 1 9 4 1 . 1 : 9 - 1 9 . 2 2 3 - 2 2 4 . S A B R O S K Y , C U R T I S , W . 1 9 7 8 . Tachinid parasites of P A T E L , R . C . , P A T E L , J . C . , a n d P A T E L , J . K . Heliothis in t h e w e s t e r n h e m i s p h e r e ( D i p t e r a . L e p i d o p • 1 9 7 3 . M a s s r e a r i n g of Chelonus heliopae G u p t a . I n d i a n tera). Proceedings of the Entomological Society of Journal of Entomology 35(2):119-126. W a s h i n g t o n 8 0 ( 1 ) : 3 7 - 4 2 . P A T E L , R . C . , a n d S I N G H , R . 1 9 7 2 . B i o l o g y a n d b r e e d • S A N K A R A N , T., and N A G A R A J A , H . 1 9 7 9 . A n o t e o n ing m e t h o d of Goniophthalmus halli Mesnil (Diptera, Eucelatoria sp. nr. armigera (Coq.) (Dip., Tachinidae), Tachinidae), a larval parasite of Heliothis armigera imported from U.S.A. for trial against Heliothis armigera. (Hubn.) Indian Journal of Agricultural Sciences 42(B) : (Hub.) (Lep., N o c t u i d a e ) i n India. E n t o m o n 4(4): 3 7 9 - 3 8 1 . 7 3 9 - 7 4 3 . SESHU REDDY, K.V., and CHANNA BASAVANNA, P A T E L , R . C . , S I N G H , R . , a n d P A T E L , P . B . G . P . 1978. S t u d i e s on t h e e s t i m a t i o n of loss in r e d g r a m 1 9 6 8 . Nuclear polyhedrosis of the gram pod borer, Helio• d u e to Heliothis armigera (Hubner). University of Agricul• this armigera. Journal of Economic Entomology 61 (1): tural Sciences Technical Series 20, Hebbal, Bangalore , 1 9 1 - 1 9 3 . India. P A T E L , R . C . , S I N G H , R., a n d P A T E L , P . B . 1 9 7 0 . B i o • S I M M O N D S , F.J. 1 9 5 8 . The successful breeding of Pal- n o m i c s of Carcelia illota ( C u r r a n ) , t a c h i n i d p a r a s i t e of pozenillia palpalis (Ald.) (Diptera, Tachinidae) a parasite Heliothis armigera ( H b n . ) larvae. Bulletin of E n t o m o l o g y of Diatraea s p p . T r o p i c a l A g r i c u l t u r e 3 5 : 2 1 8 - 2 3 4 . 11(2): 1 6 1 - 1 6 8 . S I T H A N A N T H A M , S . , a n d R E E D , W . 1 9 8 0 . Studies on P A W A R , A . D . , D I V A K A R , B.J., a n d S I N G H , S . N . t h e e x o t i c p a r a s i t e , Eucelatoria sp. ( T a c h i n i d a e , D i p te ra) 1 9 8 1 . Field r e c o v e r y of Eucelatoria sp. nr. armigera on Heliothis armigera (Hb.) at ICRISAT Center during (Coq.) (Diptera: Tachinidae) from Heliothis armigera 1 9 7 9 - 8 0 . P r e s e n t e d a t t h e T h i r d W o r k s h o p , All India C o o r • (Hubn.) (Lepidoptera: Noctuidae) in Karnataka, India. d i n a t e d R e s e a r c h Project o n B i o l o g i c a l C o n t r o l . O c t 1 9 8 0 , E n t o m o n 6(2): 1 7 5 - 1 7 7 . Punjab Agricultural University, Ludhiana, India. R A B I N D R A , R . J . , a n d S U B R A M A N I A M , T . R . 1 9 7 3 . A S K O B L O , I.S. 1 9 4 0 . T h e e c o l o g y of Habrobracon brevi- cytoplasmic polyhedrosis of gram caterpillar, H. armigera cornis, a p a r a s i t e of t h e l a r v a e of t h e c o t t o n N o c t u i d a n d (Hbn.). Madras Agricultural Journal 60(7):642-643. the possibility of its practical utilization. Reports of t h e R A W A T , R.R., J A K H M O L A , S . S . , a n d S A H U , H.R. S c i e n t i f i c m e e t i n g s of the L e n i n g r a d Institute of A g r i c u l • 1 9 7 0 . A s s e s s m e n t of l o s s e s of h y b r i d s o r g h u m C S H 1 to ture. 5 N o s . L e n i n g r a d , 1 9 4 0 . ( R u s s i a n ) . e a r h e a d c a t e r p i l l a r s , a n d c o m p a r i s o n o f i n s e c t i c i d a l c o n - trols. P A N S 16(2): 3 6 7 - 3 6 9 . S R I N I V A S A N , P . M . 1 9 5 9 . C o n t r o l of fruit b o r e r H. armig• era (Hb.) on t o m a t o . Indian J o u r n a l of H o r t i c u l t u r e 16: R E E D , W . , S E S H U R E D D Y , K.V., L A T E E F , S . S . , 1 8 7 - 1 8 8 . A M I N , P.W., and D A V I E S , J . C . 1 9 8 0 . C o n t r i b u t i o n o f I C R I S A T t o s t u d i e s o n plant r e s i s t a n c e t o i n s e c t a t t a c k . S U K H O R U C H E N K O , G . I . , N I Y A Z O O , O . D . , a n d P r e s e n t e d t o t h e S c i e n t i f i c W o r k i n g G r o u p o n t h e U s e o f A L E K S E E V , Y u . A . 1 9 7 7 . T h e effec t o f m o d e r n p e s t i • N a t u r a l l y O c c u r r i n g Plant P r o d u c t s i n Pest a n d D i s e a s e c i d e s o n b e n e f i c i a l a n d injurious i n s e c t f a u n a o f c o t t o n . C o n t r o l , 1 2 - 1 5 M a y 1 9 8 0 , N a i r o b i , K e n y a . 1 4 p p . E n t o m o l o g i c h e k o e O b o z r e n i e 56(1): 3 - 1 4 .

166 TIKAR, D.T., and THAKARE, K.R. 1961. Bionomics, biology and immature stages of an ichneumonid, Horo- genes fenestrate Holmgren, a parasite of gram caterpil• lar. Indian Journal of Entomology 23:116-124.

TWINE, P.H. 1973. Egg parasites of Heliothis armigera a n d H. punctigera in South eastern Queensland. Queens• land Journal of Agricultural and Animal Sciences 30 ( 4 ) : 3 3 1 - 3 3 6 .

TWINE, PETER, H. 1980. Proceedings, Workshop on Biological Control of Heliothis spp. 23-25 Sept 1980, Too- woomba, Queensland, Australia. 125 pp.

167 Discussion—Session 3

It was suggested that there is a great deal spoken mated to range from $1.50 to $2.50 per thousand, and written about the use of parasites for Heliothis but some commercial dealers are selling these control in many countries, including India, but there predators at considerably higher prices. Dr. Nagar- appears to be little evidence of practical utility in katti did not know of any attempts in India to spray farmers' fields. Dr. King pointed out that Tricho- artificial food on crops to augment Chrysopa spp gramma is apparently widely used in the People's activity but reported that she had successfully used Republic of China for stem-borer control in maize the yeast, Saccharomyces fragilis in the laboratory and sugar. Although chemicals are the chief for rearing Chrysopa spp. Dr. King commented that means used for the control of insects in cotton, California workers have shown that a yeast mixture there are reports that Trichogramma has also b e e n does help to increase chrysopid activity, but that it successfully used for the control of Heliothis in this does not appear to be economically feasible. crop. In discussion of the compatibility of insecticide Following a recent visit to the USSR, Dr. Chhabra and parasite use, the judicious timing of pesticide reported that he had seen a Trichogramma m a s s - use in relation to the release of parasites or preda • production unit in Tashkent that produces enough tors, or the buildup of natural enemies, was parasites to cover the release demand of 100 stressed. The use of selective pesticides that are ha/day. He had been told by the Head of the Bio• relatively ineffective against parasites and preda• logical Control Laboratory there that of 23 million tors is obviously desirable. However, Dr. Nagarkatti ha of crops in the world that are treated with Tricho- said that in her laboratory tests the use of endosul- gramma for Heliothis control, about 13 million are in fan at recommended concentrations was by no the USSR. There is a plan to switch over totally from m e a n s as safe for t h e natural e n e m i e s as is gener• chemical control to biological control with this par• ally believed. The possibility of selecting the paras • asite. Recoveries of parasites from 80% of the eggs ites for pesticide resistance was considered worth are claimed. pursuing, but Bartlett commented that if genes for Dr. King confirmed that there are definite correla• resistance to pesticides were present in many par• tions between parasitism by Trichogramma a n d asites, then they would have been selected in the host density. This is apparently related to chemi• field conditions. Efforts to select in the laboratory cals emanating from the host or host products. The had not met with much success. minimum host density level for parasitic activity has In the discussion of the potential for insect patho• not been generally determined, although levels for gen use, Bell reported that although the Autogra- specific behavioral reactions probably exist. He pha californica NPV is not as effective as the also emphasized the need continually to monitor Heliothis NPV against H. zea, it is p a t h o g e n i c to a Trichogramma and other mass-produced paras• wide range of general leaf feeders and so may be ites for vigor and essential behavioral characteris• commercially successful because of its wider tics. Experiments using hosts that lay large eggs, in market. Dr. Jayaraj had found Heliothis NPV to be attempts to produce larger and more fecund T. promising when used on chickpea where H. armig- pretiosum, have been successful. But when these era w a s the key pest; however, on Lablab niger, it parasites were compared with others in cotton did not kill a high proportion of the H. armigera plots infested with Heliothis, there were no detecta• larvae, and two other pests—M a r u c a testulalis a n d ble differences in the parasitization. Adisura atkinsoni—which w e r e not killed by this A t t e m p t s to m a s s rear Campoletis have appar• virus, were also damaging on this crop. Dr. Jayaraj ently been hindered by sex ratio problems. Dr. King also commented that the use of virus against H. pointed out that the utility of a parasite may depend armigera a n d Spodoptera litura w a s h a m p e r e d by upon using a factitious host for mass production cannibalism, predation by birds and ants, and rain. and determining the means for maintaining a suita• However, McKinley considered that predation ble sex ratio. In the long term, in vitro rearing te c h • could help the natural spread of the virus and so n i q u e s m a y be of possible use. could be useful. In discussions of the use of predators, the cost of Dr. Rothschild wished to record a plea for a more m a s s p r o d u c t i o n of Chrysopa in the USA was esti• quantitative approach to biological control. The

1 6 8 percentage parasitism or counts of predators are meaningless in the absence of knowledge of what contribution the individual species of natural ene• mies make towards the restriction of pest survival. A small change in an otherwise low parasitism at a critical stage may be more effective in regulating pest populations than a high parasitism at a less critical stage.

169

Session 4

Chemical Pesticides: Their Uses and Abuses

Chairman: T.S. Thontadarya Rapporteurs: C.S. Pawar Cochairman: A.G.L. Wilson S.L. Taneja

A Critical Review of the Role of Chemical Pesticides in Heliothis Management

R.J.V. Joyce*

Abstract

The genus Heliothis, which includes key pests of many major crops such as cotton, tobacco, and maize, has probably been more responsible for the greater use and abuse of insecticides than any other insect. More than any other genus, it has been responsible for the formulation of the integrated pest management concept, because of failures, in many parts of the world, of control by standard crop-spraying procedures. H e l i o t h i s spp are essentially r-strategists, adapted to survive in unstable habitats, which they are able to discover through the great mobility of the adults and exploit through the polyphagous habit of the larvae. The strategy of crop chemotherapy is unsuitable for protecting crops against attack by such species, and attempts to employ it have generated the problems now faced. The development of an agroecosystem within an unstable ecosystem introduces more stability, and thus reduces the effectiveness of the major factor regulating the numbers of r-strategists. Catastrophic pest outbreaks in the crops can be prevented only by operating some new factor against the pest. In the case of Heliothis spp, insecticides provide the only immediate factor, but they are environmentally acceptable and economic if they kill only the necessary numbers of those stages generating the damaging fraction of the total population of the species, with the minimum impact on other organisms. This requirement calls for physiological or ecological selectivity. The advantages and disadvantages of the various stages of the Heliothis life cycle as targets for insecticides are discussed in relation to the insecticides available and their selectivity. Experience in protecting the cotton crop in Sudan from attack by H. armigera by killing adults, chosen as the best target stage, is described.

*Formerly of the Agricultural Aviation Research Unit, Crantleld.,UK,

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management 15-20 November 1981, Patancheru, A.P., India. 1 7 3 T h e g e n u s Heliothis has a worldwide distribution in about the received dose, because losses to surfa• tropical and subtropical regions. H. zea o c c u r s in ces other than those of the crop are ignored; nor is the New World from Canada to Uruguay and H. account taken of the distribution of deposits in rela• armigera, which differs from H. zea only in the tion to the three-dimensional properties of the crop. minute structure of the male genitalia, is found in In fact, the received dose is highly variable within southern Europe, the whole of Africa, the Near and the crop on any occasion, and at any level on Middle East, the Far East, Australia, New Zealand, different occasions. Consequently, the stated and many of the Pacific Islands. These two species objective—an even cover—is never achieved. of a genus containing at least four more major pest Moreover, the objective itself is highly questiona• species, have probably been responsible for the ble and certainly inefficient in the use of pesticides. use and abuse of more insecticides than any other For example, the recommended applicance of insects. This is because they are major pests of DDT is 1 kg/ha. The economic injury level often is important crops, such as cotton, tobacco, and reached when there are 10 larvae per 100 plants, maize in many parts of the world, including the USA, and over 90% of the plants are still uninfested. Th e which consumes some 45% of all pesticide pro• crop will enjoy maximum protection if these larvae duction and nearly 50% of this on cotton (Furtick are killed before they do any damage, that is, on 1976). This overuse of insecticides on cotton in the eclosion, when their total weight is about 10 g/ha. Americas led, more than any other event, to the The theoretical amount of DDT required to kill this designation of the "disaster phase" of Luckman many larvae is about 10µg; we apply 109 µg/ha. It is and Metcalf (1974) and the evolution of the inte• difficult to conceive a strategy for chemical control grated pest management (IPM) concept. However, less efficient in the use of pesticides, and a greater despite the major efforts being devoted in the USA environmental burden. to control pests of major crops by cultural, biologi• We must also enquire whether such crop che• cal, and genetic means and by plant breeding, the motherapy can be regarded as pest management, control of Heliothis spp in that country still relies which I take to mean "the regulation of pest heavily on crop spraying of synthetic insecticides. numbers." Certainly, we may kill a high, or very high I shall attempt to show in my paper that insecti• proportion of the pest species present in the crops cides will continue in the foreseeable future to be treated, and by residual toxicity kill some of the later essential for protecting crops against such pests invaders. Whether this procedure regulates the as Heliothis. It is not insecticides per se that are pest population depends on what fraction of the responsible for the problems that have arisen, but total area occupied by the population is treated at the strategy, and tactics employed, which have one time. As Knipling (1972) states, "100 percent failed to make use of available knowledge of the control on 99 percent of the host acreage falls far basic ecology and behavior of the species con• short of the suppression that is achieved when 90 cerned. That is to say, for the most part, insecti• percent control is obtained on 100 percent of the cides in this case have been directed at the wrong host acreage." There is no evidence that the crop target, at the wrong time, and in the wrong way. chemotherapy now practiced has ever regulated A critical review of the role of pesticides in Helio- populations of Heliothis spp anywhere except on a this management cannot fail to conclude that this time scale measured in days in small fractions of has been confined to a strategy of crop chemother• the area occupied. apy that aims at maintaining the crop as an envir• We cannot speak of pest management by chem• onment lethal to the pest species. The icals or any other means until we define the popula• performance specification given to the farmer or tion that has to be managed, and measure its crop-protection agent is to spread a recommended distribution in space. This distribution is subject to quantity of pesticide over all crop surfaces—the constant change. Taylor and Taylor (1977) con• "applicance" of Hartley and Graham-Bryce (1980). sider it necessary to treat the anatomy of a real Applicance (kg/ha, for example) states nothing population as being three-dimensional—latitude x

174 longitude through time, but having an internal retic• tems, population dynamics, and dispersal, though ulate structure analogous to that of a fern stele (Fig. —as Taylor et al. (1980) point out in respect of 1). migrant pests in the United Kingdom— Pest management, as emphasized by Rabb "Conventional population dynamics has so far (1970), is rooted in ecology, and deals with ecosys - been of little value...because it is mainly concern e d with temporal, not spatial change." It may also be added that most work on insect migration does not help much, since it deals primarily with exodus, while we are more concerned with entry into a habitat. The theme of this paper is that while chemical pesticides are regularly employed in protecting crops against damage from Heliothis spp, they have, almost without exception, been used ineffi• ciently to execute a strategy inappropriate for the ecology and behavior of the species. Accordingly, the intial easy successes of the strategy have fre• quently been followed by breakdown in control, through the emergence of strains highly resistant to a great range of chemicals (Wolfenbarger et al. 1971; Adkisson 1972) and resurgence of infestation following destruction of natural enemies (Kni- pling 1979). The problems engendered by this crop chemotherapy might be largely surmounted if an insecticide were evolved that selectively kills Heliothis without damage to natural enemies. Chlordime- form most closely approaches this ideal. The nuclear polyhedrosis virus, Baculovirus heliothis (Smith et al.1978; Luttrell et al. 1979), is also pr o m • ising, but is unlikely to be able to control severe outbreaks (Bull et al. 1979). Such insecticides, however, would still not provide pest management unless they were used in a strategy suited to the pest's ecology and behavior. This understanding is the first requirement. Moreover, with such under• standing, existing chemicals may find a place in management of the pest if applied by methods that are ecologically selective. I will describe recently elucidated aspects of the ecology of H. armigera in the Sudan Gezira and how pesticides were used, with considerable ecological selectivity, to regulate the numbers of the pest so that economic injury levels were not reached in the crops at risk.

The Ecological Basis of Heliothis Management

Figure 1. Conceptual model for pest popula• The Objective of Pest Management tion anatomy. Based on Rostowzew's drawing of the stelar structure of the adder's tongue The objective of pest management is to prevent a fern. (Source: Taylor and Taylor 1977). species occurring in crops in numbers, and at a

175 time w h e n they c a n c a u s e u n a c c e p t a b l e c r o p loss. e n v i r o n m e n t s that p r o d u c e habitats having a low W h e n c h e m i c a l insecticides are u s e d , they must d e g r e e of predictability a n d p e r m a n e n c e , so it is be applied in s u c h a w a y as to a c h i e v e (1) the not surprising that indigenous insects possess a greatest e c o n o m y a n d (2) the m i n i m u m effect on high d e g r e e of migratory activity that enables t h e m nontarget organisms. W e are not necessarily c o n • to seek out s u c h short-lived opportunities as well c e r n e d with regulating entire populations, but in as to e s c a p e from d o o m e d ones, a n d a high intrin• identifying that f r a c t i o n of t h e total population that sic rate of increase, w h i c h permits t h e exploitation we must control to prevent d a m a g i n g infestations of these habitats. from occurring. This objective requires understanding of the origins of the fraction of the population that p l a c e s Mobility of Heliothis Moths the c r o p at risk, a n d the n u m b e r a n d distribution of t h e stage or stages that, if killed, will prevent the Heliothis spp are highly mobile a n d highly f e c u n d , o c c u r r e n c e of this fraction. Adults of Dysdercus a n d their larvae are p o l y p h a g o u s (cf. H a r d w i c k fasciatus, for e x a m p l e , colonize a c o t t o n field a n d , 1965; Callahan et al. 1972; Sparks et al. 1975). as a result of feeding on a suitable host, lose their T h e y are well a d a p t e d to exploit unstable habitats wing m u s c l e s by autolysis. D a m a g i n g infestation a n d versatile in their life strategies. T h e fecundity d e v e l o p s f r o m the multiplication of these initial a n d longevity of H. armigera have been s h o w n by immigrants thus t r a p p e d in the crop. Their destruc• Hackett (1981) a n d T o p p e r (1981) to be a function tion provides c r o p protection. Similarly, d a m a g i n g of the quality of their foods, w h i c h must include levels of infestation of jassids a n d whitefly are also a m i n o acids. During three seasons, T o p p e r (1981) normally g e n e r a t e d by small n u m b e r s of i m m i • never r e c o r d e d in any c r o p m o t h densities e x c e e d - grants breeding in the crop. If their rate of increase ing 1 0 0 / h a , a n d in all crops, n u m b e r s c h a n g e d c a n be predicted, they m a y be destroyed by suit• f r o m day to day a n d hour to hour. He c a l c u l a t e d that able c r o p c h e m o t h e r a p y before they r e a c h these the m e a n n u m b e r of eggs laid e a c h night w a s about levels ( J o y c e 1959, 1961), but only if treatments are 5 2 0 / h a per female. T h u s 3 0 m o t h s / h a c o u l d g e n • on a s c a l e c o m m e n s u r a t e with the insects' mobil• erate d a m a g i n g levels of larvae if half were ovipos• ity. T h e d a m a g i n g fraction of t h e population is that iting females. W h e n food w a s abundant, flight w h i c h o c c u r s in the c r o p s at risk. This type of life activity was s u p p r e s s e d , with m o t h s e n g a g i n g only strategy h a s g e n e r a t e d t h e c o n c e p t of e c o n o m i c in short flights during the first 3 days after e m e r • threshold, defined as the level of infestation at g e n c e , after w h i c h they r e a c h e d sexual maturity. w h i c h control must be applied to prevent the o c c u r • M o t h s e n g a g e d in prolonged flight ( u p to 7 2 0 m i n • r e n c e of t h e e c o n o m i c injury level (Stein et al. utes in the laboratory) only if they derived from 1959). In contrast, locusts, for e x a m p l e , c a u s e larvae f r o m poor host plants a n d h a d poor quality d a m a g e by invasion in n u m b e r s far in e x c e s s of the f o o d during this first 3 d a y s of life (Hackett 1981). e c o n o m i c injury level, a n d protecting c r o p s against U n d e r s o m e conditions, therefore, infestations of H. these insects d e m a n d s m e a s u r e s very different armigera m a y be largely derived from distant sour• from c r o p c h e m o t h e r a p y . T h e d a m a g i n g fraction c e s ; under others, nearby s o u r c e s alone are impor• m a y be g e n e r a t e d a n y w h e r e in the distribution area t a n t . N e v e r t h e l e s s , all m o t h s e n g a g e i n of the species, so that t h e entire w o r l d population of short-distance flight, up to 8 0 % of the night hours the s p e c i e s is potentially d a m a g i n g a n d must be being spent airborne in s e a r c h of f o o d a n d oviposi- controlled. tion sites (Topper 1981). In the S u d a n Gezira, there

We must enquire w h e r e Heliothis fits into the w a s a nightly m o v e m e n t from groundnut, w h e r e s p e c t r u m of life strategies. most of the m o t h s had developed, to a flowering l e g u m e , Lens cajan, for nectar, t h e n c e to cotton for oviposition, a n d back to groundnut for resting in the Heliothis Spp as r--Strategists daytime. During these flights moths are invariably oriented "Habitat is t h e t e m p l a t e against w h i c h evolutionary d o w n w i n d , a n d thus c a n m o v e in a single night pressures f a s h i o n t h e e c o l o g i c a l strategy of a s p e • several kilometers f r o m their resting site of the cies. T h e instability:stability s p e c t r u m gives rise to previous day. Infestation levels t e n d to be dis• t h e r-K selection continuum of MacArthur (1960)," p l a c e d d o w n w i n d . Moreover, in the S u d a n , steady says S o u t h w o o d (1974). C o t t o n is a c r o p g r o w n in e v e n i n g w i n d s are often replaced at this t i m e of t h e

176 year by disturbances such as convectional storms A and the passage of the intertropical discontinuity (ITD). The ITD was found capable of concentrating airborne insects by nearly 3 0 % / h o u r (Rainey 1974, 1976). The cold outflows from storms, which often occur at times of maximum insect flight, were shown by Schaefer (1976) to produce a 60-fold increase in airborne insect density at a sharply defined front some 30 km ahead of the rain (Figs.2, 3). The effect of this on the displacement and sub• sequent oviposition of H. armigera has been de• scribed at this workshop (Haggis, these Proceedings).

Origins of Damaging Infestation Levels

Damaging larval infestations on cotton in the Sudan Gezira thus derive from highly mobile sour• B ces, so that, in any one field, new and variable infestations occur each day. Due to the ebb and flow of populations, large areas may have common infestation levels but the boundaries of these areas show rapid and abrupt change (Figs. 4, 5). In the Sudan Gezira the breeding of H. armigera on cotton was found to make only a small contribution to infestation levels, most of the moths immigrating into a field having come from other sources, such as groundnut or sorghum. In contrast, Lawson (1980) found that rainfed cotton in Thailand, once colonized by moths bred in maize, generated its own damaging populations, though flight activity probably resulted in redistribution of population over at least several kilometers, particularly from older cotton. Studies such as these show clearly that damag• Figure 2. Beginning of evening takeoff of ing larval populations cannot be assumed to derive insects in the Sudan Gezira: mainly Noctuid from the same fields as those in which the parent moths (Heliothis armigera, Spodoptera littora- moths had bred, even if, as in Thailand, fields were lis, etc.). Kumor,11 Oct 1973; range-rings 450m several hundred hectares in area. In Sudan, the 1 0 apart. A, 1806; single exposure at 1 /2 elevation. smooth change in the daily mean levels of oviposi• B, 1808; triple exposure at 3° elevation. tion over the whole Gezira (Haggis, these Proceed• (Source: Schaefer 1976, with acknowledg- ings) suggests the flux of a single population over ments to Blackwell Scientific Publications, several thousands of square kilometers. In this Oxford, UK, and the Royal Entomological sense, Heliothis may be considered a migratory Society of London.) insect.

Choice of Stage to be Attacked before they do the damage. The food intake of The control of migratory pests may be sought either Heliothis larvae increases exponentially with age, by killing them in their source areas or en route to, but the number of buds of cotton plants damaged or on arrival in, the crops at hazard. Clearly, if c r o p per day varies little, since young larvae attack protection is to be maximized, they must be killed small, and older larvae large, buds (Russell-Smith,

177 A B C

D E

Figure 3. Insects at a storm-outflow cold front Probably mainly A i o l o p u s . Radma, Sudan ,19 Oct 1971; single exposures. A. 2013; range-rings 7.5 km (8000 yd) apart and elevation 3°; rain-storm centered 35 km away to northeast and cold outflow at 8 km, also approaching from northeast, 1 0 undercutting warm southwest wind. B. 2026; range-rings 450 m apart and elevation 1 /2 ; note dense leading edge of cold outflow approaching from northeast and now 850 m away; canal bank also shown, running southeast-northwest to southwest of radar site, and outlines of fields. C. 2028; range-rings 450 m apart; looking up at 30° elevation at very sharply defined leading edge as it reaches the radar; frontal slope of about 1 in 2 demonstrated by shape of sector of high-density 1 0 echoes. D. 2041; range-rings 7.5 km apart and elevation /2 ; cold outflow now 8 km away, receding to southwest, and with a visible length of at least 60 km. E. 2050; range-rings 7.5 km apart and 1 0 elevation 1 /2 ; cold outflow 13 km away, still receding to southwest, and visible to at least 45 km: storm collapsing period. (Source: Schaefer 1976, with acknowledgements to Blackwell Scientific Publications, Oxford, UK, and the Royal Entomological Society of London.) unpublished). Therefore, the latest stage that can 1. The crop is made more or less lethal to species be attacked to maximize crop protection is the associated with it, especially parasites and preda• first-instar larvae on eclosion, though it is neces • tors of Heliothis eggs, larvae, and pupae. sary to examine whether more economical pest 2. Heliothis larvae, being polyphagous, are richly management may be achieved by attacking earlier endowed with multifunctional oxidase enzymes, stages in the development of the damaging which provide the chemistry for the development of population. resistance to insecticide (Wilkinson 1968; Dahms In contrast to this strategy, it is customary to and Nakatsugawa 1968; Cassida 1970; Brooks establish a threshold level of larval infestation a n d 1972). then to treat the crop so that all surfaces are given a 3. Sublethal deposits are always available due to deposit lethal to the species, and so prevent estab • uneven distribution, degradation, and expansion of lishment of the pest within the crop. This procedur e plant surfaces. has many disadvantages besides those already 4. The crop grows, and new eggs are laid on uncon- emphasized, the most important being: taminated foliage.

178 No. of eggs/100 plants (22-24 Sept 1975)

HUDA

CENTRE WAD MEDANI

MANAGIL

SOUTH

0 10 20 30

Ki lometers Mean/100 plants

2 - 4

4 - 8

8 - 1 6

1 6 - 3 2

Figure 4. Distribution of Heliothis armigera eggs on cotton in the Sudan Gezira, 22-24 Sept 1975.

179 No. of eggs/100 plants (25-27 Sept 1975)

CENTRE WAD MEDANI

MANAGIL

SOUTH

0 10 2 0 3 0

K i l o m e t e r s Mean/100 plants

2 - 4

4 - 8

8 - 1 6

1 6 - 3 2

Figure 5. Distribution of Heliothis armigera eggs on cotton in the Sudan Gezira, 25-27 Sept 1975.

180 5. Unacceptable larval infestations can rarely be discovered and destroyed before they have perpe• Table 1. Dossage-mortality relations against L3 larvae trated more than half of their potential damage. of H. virescens a n d H.ZES. B e c a u s e of these inadequacies, I do not propose to A c t i v e i n g r e d i e n t discuss larvicides further. They have only a limited µ g / g role to play in Heliothis management, although the M e t h y l p a r a t h i o n 9 . 5 9 vast majority of the hundreds of journal papers M e t h o m y l 1 7 . 0 4 consulted deal with this strategy, which indeed, Monocrotophos 2 1 . 8 7 appears to represent the standard method of eva• Toxaphene-methyl parathion (2:1) 3 4 . 4 0 luating the performance of new insecticides Toxaphene-methyl parathion (3:1) 6 9 . 6 5 against the species. The attractive stages for Toxaphene-DDT 2 1 7 . 6 0 attack are the adult and the egg, and these will now be discussed. Source: Lentz et al. 1974.

Targets for Insecticides adults as targets for insecticides are emphasized. Adults may be killed by direct contact, indirect Heliothis Adults as Targets contact and vapor action, and by stomach entry. Stadelbacher et al. (1972) caged H. virescens a n d Adult Noctuids are particularly attractive tor insec- H. zea on cotton plants 24, 48, and 53 hours after ticidal control. Dittrich et al. (1980) found that larval their terminals had been sprayed with either mono• resistance against monocrotophos in an R (resist• crotophos, carbaryl + molasses, carbaryl- ant) strain of Spodoptera littoralis is characterized toxaphene + methyl parathion, or toxaphene-DDT. by 250x difference of LD50, compared with the Mortality among moths was significantly greater on sensitive (S) strain. Similarly, Wolfenbarger and all sprayed than on unsprayed plants, except those McGarr (1970) found that the LD50 of methyl para- treated with toxaphene-DDT, when moths were thion to larvae of H. virescens reared from material introduced 24 and 48 hours after treatment. Fifty- collected from the field late in the season was 20 three hours after treatment, significant mortality times higher than that to larvae collected early in was found only on plants sprayed with carbaryl + the season. Wilson (1974) showed that the Ord molasses and monocrotophos. Valley strain of H. armigera, which had been In the Sudan Gezira, where the applicance is 300 exposed to repeated sprays containing DDT, had g m o n o c r o t o p h o s / ha, the median deposit of active 35-fold tolerance to DDT-toxaphene, 5-fold toler• ingredient on the cotton terminals immediately ance to methyl parathion, and 4-fold tolerance to after spraying is about 300 (+ 120) ng/cm2 , a n d the endosulfan. According to Dittrich et al. (1979), this deposit has a half-life of about 24 hours. This small ability to develop resistance to metabolic toxicants applicance is adequate to make a substantial con• is based on the presence in the larvae of at least tribution to the mortality of moths visiting the cro p two mechanisms: an efficient system of MFO 12 hours after spraying, because the moths, enzymes and an insensitive cholinesterase actively settling on one plant after another during (AChE). In moths, the resistance to the insecticides feeding, mating, and oviposition, presumably was much lower than in the larvae, and it appeared accumulate a toxic dose. Accordingly, mortality is that the moth lacked the powerful MFO system, greatest among ovipositing females (Topper 1981). leaving only the insensitive AChE as the R mecha• In the laboratory, Lawson (1980) found that depos- nism, so that tolerance was able to develop only its of monocrotophos as low as 50 ng/cm2 killed about 2- to 4-fold. 5 0 % of laboratory-bred H. virescens in 15 hours. Though data are scarce and inadequate, the He also found that direct application of profenofos moths appear to be 10 to 100 times more sensitive at 3 µg/g against the same species gave 50% to insecticides than S and R larvae, respectively. mortality in 48 hours. Table 1 gives the LD50 levels of insecticides widely Uk and Outram (1979) investigated the contami• u s e d in Heliothis control in the USA and treated nation of the subbracteal nectar of G. hirsutum, against laboratory-reared larvae (Lentz et al. 1974). variety Acala, in the Sudan Gezira followng the When we consider the changes in these levels to application of monocrotophos at 300 g ai/ha. They be expected from the R factor, the advantages of found that this approximated to 2 ppm, and that the

181 contamination had a half-life of about 3.5 days. Laboratory studies by Bourgeois (unpublished) Table 2. Ovlcidal activity of Insecticides against eg g s o f H. virescens on cotton, 1979. provided an LD50 of monocrotophos to H. virescens through stomach action at about 100 ppm. If feeding makes a contribution to mortality of H. Applicance Eggs h a t c h i n g armigera moths in the field, either they are more Insecticide ( k g / h a ) <%) susceptible than the laboratory strain of H. virescens tested, or they can accumulate a toxic dose through voracious feeding. According to Outram M e t h o m y l 0 . 1 3 8 4 0 . 0 3 4 2 6 (unpublished), adult H. armigera h a v e b e e n 0 . 0 6 9 3 1 observed to take in as much as 0.5 ml of sugar solution in 24 hours. This is the right order of ma g n i • T h i o d i c a r b 0 . 1 3 8 4 5 tude of food intake to enable some moths to 0 . 0 6 9 5 4 accumulate a toxic dose from contaminated nectar 0 . 0 3 4 6 2 in a single night. Chlordimeform 0 . 1 3 8 6 1

Eggs and L1 Larvae as Targets P e r m e t h r i n 0 . 0 5 5 6 3 0 . 0 1 4 7 9 0 . 0 2 8 8 4 When eggs are targets for destruction, it is of little economic significance whether the insecticide is a Methyl parathion 0 . 1 3 8 6 4 true ovicide or destroys the L1 larvae immediately after eclosion, when the young larvae characteris• Fenvalerate 0 . 0 5 5 6 9 tically eat at least part of their egg shell and som e of 0 . 0 1 4 8 8 the leaf tissue in the immediate vicinity. Pitts an d 0 . 0 2 8 8 0 Pieters (1980) assessed various ovicides in terms of the percentage of eggs that hatched on sprayed P r o f e n o f o s 0 . 1 3 8 7 0 cotton (Table 2). In subsequent field trials, methomyl was consistently the best ovicide at all C o n t r o l 9 6 rates. On the basis of Sudan data, the applicance used in these experiments could be expected to Source: Pitts and Pieters (1980). provide deposit densities of less than 500 ng/cm2 , but no measurements were reported. No precise data have been found on the susceptibility to insecticides of L1 larvae on eclosion, but evidently they are easily killed. Sudan data indicate employed if they can be directed against moths on that 99% mortality can be expected from larvae a scale commensurate with their nightly move• emerging from eggs laid on leaves contaminated ments. Similarly, eggs, which have an incubation with monocrotophos to a level of about 2 ppm; time rarely more than 4 and often less than 2 days, probably they are also equally susceptible to many are a practical target only if they are laid synchro • other larvicides. This would equate to about 1µ nously over the areas to be treated, or if the ovicide g/cm2 or about one-tenth of the quantity needed to has a persistence commensurate with the duration kill an L3 larva by direct contact. of the period of oviposition. The question of scale Clearly, eggs and L1 larvae represent targets far must then be resolved. Secondly, insecticides and more attractive than later larval stages, but other methods of application have to be selected to min• aspects that emerge only from large-scale opera• imize the effects on nontarget organisms tions must be considered. In the context of the latter, the physiological selectivity of chlordimeform is of special interest. The chemical is rapidly absorbed into the plant Adulticides and Ovicides in Field Use tissue (Ware et al. 1975), from which it is evidently released through the stomata as a vapor. It must be Since adults are highly mobile and carry their eggs assumed that this vapor accumulates in the leaf with them, adulticides will be most economically boundary layer, the thickness of which is measured

182 in urn, to concentrations that are lethal to species agement that carries the responsibility, among oth• utilizing this layer. These include young Noctuid ers, of protecting the cotton crop against pests. larvae. Most species of parasites and predators are little affected by chlordimeform. Sublethal concen• trations also have potentially important effects. Sources of H. armigera Infestation on Lund et al.(1979) found that, while larvae of the Cotton tobacco hornworm, Manduca sexta, were rather insensitive to insecticidal action (LD5 0 to L2 700 The southern part of the Gezira, where annual rains µg/g), at doses as low as0.24 ng/g, larvae showed exceed 450 mm, nearly 80% of which falls in July signs of intoxication, such as tremors and lack of and August, is an island of irrigated crops within a coordination. This reduced feeding (Campbell et al. vast sea of host plants of H. armigera (chiefly wild 1979), larvae often spinning down and dropping and cultivated sorghum spp), an area of thousands from the plant. Adults, which could be killed with 3.3 of square kilometers. Management of the pest in its µg/g by injection, were equally excited by sublethal source areas is unlikely to be practical or eco• doses, with reduced mating (Campbell et al. 1979) nomic. Work by Hackett (1981) and Topper (1981), and fecundity (Lingren et al. 1976). These effects however, showed that irrigated cotton and on behavior have important implications for chemi• sorghum generated an insignificant fraction of the cal control. Larvae dropping from host plants are larval infestations that damaged cotton, but in the exposed to new hazards from both physical and years under study, the irrigated groundnut crop biological environment, the latter being particularly was the major source, so that moth invasion of important, because the cause of excitation has little cotton could be predicted by the numbers of fully effect on predators and parasites. grown larvae in that crop during the previous 10 days. The opportunity therefore exists for manage• ment of H. armigera through destruction of the potentially damaging fraction of the total population at its source, at least in some years, but no trials of Target-Specific Methods of this strategy have yet been possible. Moreover, Pesticide Application in lentils, which are grown around the edges of cotton Commercial Practice fields, appear to be a preferred source of nectar, and their contamination might be usefully explored as a means of control.

My argument is that chemicals cannot provide the Airborne insects are particularly attractive management of highly mobile pests such as Helio- targets for insecticides (Rainey 1974) because Ihis spp if their use is confined to treating individual many of the species investigated have been found crops at hazard. On the contrary, chemicals are to compose the major part of the biomass in the needed to reduce the numbers of those stages, the airspace selected by their life strategy to lead to destruction of which will prevent the occurrence of survival—examples are locusts, grasshoppers, unacceptable infestations in the crop. Whether certain species of aphids, spruce budworms, etc. these stages are attacked at the source, en route Radar, light-trap, and direct observations of the to, or on arrival in, the crops, a requirement of this flight behavior of H. armigera in the Sudan have strategy is that the scale on which the insecticide is shown, however, that only a small fraction (proba• applied has to be determined by the biology and bly less than 5%) of H. armigera adults fly above a habits of the pest species and the agronomy of the height of 10 m, and, under the conditions of the area, rather than by field or farm boundaries. A Sudan Gezira, the remaining 90% are engaged in second requirement is that the insecticide must be feeding, mating, and oviposition. This lower layer of transmitted selectively to the total population of t h e air is occupied at the same time by so large a target stages with minimum loss to nontarget number of insect species, many of them predators, surfaces. that H. armigera moths represent only a minute fraction of the total airborne biomass. It would be I will illustrate this approach by describing our difficult to devise a system of insecticide applica• experience in the management of H. armigera on tion that would kill only these moths; accordingly, cotton in the Sudan Gezira—an area particularly destructon of H. armigera moths en route is not appropriate for this type of work because its million likely to be a sound management strategy. hectares of irrigated crops are under a single man•

183 Management Strategy Adopted for H. armigera GROWING POINTS The choice made was destruction on arrival of the YOUNG LEAVES 16-35% Upp Surface population immigrating into the crop. The presence 34.91% of eggs was selected as an indication of the recent presence of adults, though Lawson et al. (1979) TOP LEAVES showed that surveys for adults were equally practi• Upp Surface cal. Both methods called for daily sampling of the 28.30% whole area at risk, and therefore, for economic and statistically reliable methods for areas of hundreds of square kilometers containing over 100 thousand hectares of cotton. After analyzing the variability of egg numbers on single plant organs, on plants within rows, rows within 0.15-ha plots, plots within 4-ha holdings, holdings within 40-ha fields, and fields within administrative blocks up to 2000 ha, Russell-Smith (1975) calculated a sampling plant that provided an acceptable 20% standard error. Some of the results of these surveys are given in Figures 5 and 6, where it can be seen that areas of several hundred square kilometers had the same level of egg infestation, which had to be sprayed in the 2-day incubation period. The spray procedure was designed so that the cotton terminals where most eggs are laid (Fig. 6) were contaminated with at least 40 ppm of mono-

crotophos which, under Sudan conditions, would Period 269 - 14-10-72 Total No of Eggs 318 provide a toxic dose to emerging L1 larvae over a period of 4 to 5 days (Joyce 1978). The greatest Figure 6. Distribution of eggs of American boll- contribution to the deposit on the growing points, on worm on cotton plants, Sudan Gezira. which over 70% of the eggs were laid (Russell- Smith 1975), was made by droplets 40 to 60 Mm in diameter, which were collected efficiently by H. armigera adults. Accordingly, spraying monocrotophos at 300 to 350 g ai/ha was found to kill over more exposed to the spray cloud. Similar mass 98% of the moths present in the crop at the time, disturbances by aerial spraying were noted by and an equal number immigrating into the crop Wardhaugh during his radar obsevations in Austra• during the evening of that day. This moth destruc• lia (personal communication). Because of the sus• tion brought oviposition on cotton to an abrupt halt. ceptibility of adults to insecticides, Lawson Moreover, this depletion of the overall H. armigera (unpublished) found it possible, in operations in population was followed 10 to 14 days later by Kenya, to reduce the applicance to 230 g ai/ha. reduced larval infestation on sorghum and ground- Hull (1980) conducted a large-scale trial in nut, which were not sprayed (Topper 1981). Sudan over about 1500 ha of cotton in which the The causes of moth mortality were investigated spray program was determined by scouting for by Lawson (1980b) and Uk and Outram (1979). The adult moths, against which the spray was subse• latter found that the secretions from the extrafloral quently directed. Mortality among moths is shown nectaries on cotton contained enough insecticide in Table 3. Subsequent larval numbers, and conse- to provide a lethal dose to moths feeding for a qent damage in the area treated in this way, com• single night. Lawson showed that both direct and pared favorably with what was achieved by indirect contact action made their contributions. He directing spray at the cotton terminals (Table 4), but observed that the moths were disturbed by aircraft adults as targets required nearly 25% less noise, as well as by the spray, and thus became c h e m i c a l .

184 5.0 O l d G e z i r a Synchronized control

Conventional spraying M a n a g i l Synchronized control O l d G e z i r a

4.0 Conventional spraying

Synchronized control

3.0 M a n a g i l

O l d G e z i r a

2.0

•Managil

Conventional

1.0

0 J a n u a r y February March A p r i l

Figure 7. Accumulated monthly yields of seed cotton (G. barbadense), 1975-76 season, from areas in which pest control was based on synoptic survey and synchronized control versus conventional practice.

185 the need to reduce the amount of spray directed at Table 3. Percent mortality of ovipositing H . a r m i g e r a the cotton crop and to explore further the possibility in cotton in the Sudan Gezira after spraying with 2 3 0 g of m a n a g i n g Heliothis armigera n u m b e r s by al/ha of profenofos. attacking them away from the cotton crop.

Mortality of ovipositing moths References (%) First night Second night S p r a y d a t e after spraying after spraying ADKISSON, P.L. 1972. The integrated control of insect pests of cotton. Pages 175-188 in Proceedings, Tall 2 O c t 7 9 7 3 1 0 0 Timbers Conference on Ecological Animal Control by 7 O c t 7 9 8 2 1 0 0 Habitat Management, 4. Tallahassee, Fla, USA. 1 2 O c t 7 9 (not available) 90 BROOKS, G.T. 1972. Pathways of enzymatic degrada• tion of pesticides. Pages 106-164 in Environmental qual• Source: Hull (1980) ity and safety (eds F. Coulston and K. Korte). New Y o r k , USA: Academic Press.

BULL, D.L., HOUSE, V.S., ABLES, J.R., and MORRI• SON, R.K. 1979. Selective methods for managing insect Table 4. Mean number of eggs and larves of H . armig- pests of cotton. Journal of Economic Entomology 72(6): e r a per day par 100 plants recorded on cotton in the 841 - 8 4 6 . Sudan Gezira when sprayed (A) against ovipositing moths and (B) to contaminate plant terminals for de- CALLAHAN, PS., SPARKS, A.N., SNOW, J.P., and struction of L1 larvae (22 Sept-22 Oct 1979). COPELAND, W.W. 1972. Corn earworm. Vertical distri• bution in nocturnal flight. Environmental Entomolog y 1: 4 9 7 - 5 0 3 . A a B CAMPBELL, W.R., COUNSELMAN, C.J., and RAY, Heliothis (Mean over ( M e a n o v e r H . W . 1 9 7 9 . Evaluation of chlordimeform (Galecron® ) for stage 1500 ha) 1 0 0 0 0 h a ) Heliothis virescens control on cotton. In Proceedings, Beltwide Cotton Producers' Conference, Phoenix, Ariz, E g g s 2 . 5 6 . 2 USA. Small larvae 0.5 1 . 3

Large larvae 0.2 0 . 8 CASSIDA, J.E. 1970. Mixed function oxidase involve• ment in the biochemistry of insecticide synergists. J o u r • Source: Hull (1980) nal of Agricultural and Food Chemistry 18: 753. a . Procedure (A) used 25% less insecticide DAHMS, P.A., and NAKATSUGAWA, T. 1968. B i o a c t i - than procedure (B). vation of insecticides. Pages 89-110 in Enzymatic oxida• tion of toxicants (ed. E. Hodgson). Raleigh, NC, US A: North Carolina State University Press

DITTRICH, V., LUCTKEMEIER, N., and VOSS, G. Results 1979. Monocrotophos and profenofos: two organophosphates with a different mechanism of action in resistant The value of this approach to the management of races of the Egyptian cotton leaf worm Spodoptera liltora- lis. Journal of Economic Entomology 72: 380-384. H. armigera with insecticides is shown by the yields

of seed cotton when compared with those from DITTRICH, V. LUCTKEMEIER, N., and VOSS, G. conventionally sprayed areas (Figure 7). Moreover, 1 9 8 0 . OP—resistance in Spodoptera litloralis: inherit- much of the increased yield came from earlier ance, larval and imaginal expression and consequenc e s picks, which provide the best grade of cotton. for control. Journal of Economic Entomology 73:356- 3 6 2 .

Since 1977, the situation in the Sudan Gezira has FURTICK, W. R. 1976. Insecticides in food production. been complicated by the introduction of a new Pages 1 -15 in The future of insecticides, volume 6. (Eds. s p e c i e s of c o t t o n , Gossypium hirsutum variety R.L. Metcalf and John J. McKelvey). John Wiley Seri e s i n A c a l a , replacing G. barbadense variety Barakat, Advances in Environmental Science and Technology, and catastrophic increase in whitefly (Bemisia New York, USA: John Wiley.

tabaci) damage. The potential importance of par• HACKETT, D.S. 1981. Studies in the biology of Helico- asites and predators in controlling this pest and its verpa armigera in the Sudan Gezira. Ph.D. thesis, Univer• intractability to control by insecticides emphasize sity College of North Wales, Bangor, Wales, UK.

186 HAGGIS, M.J. 1981. Spatial and temporal changes in LINGREN, P.D., and WOLFENBARGER, D.A. the distribution of eggs of Heliothis armiger ( H u b n e r ) 1976. Competition between Trichogramma pretiosum (Lepidoptera: Noctuidae) on cotton in the Sudan Gez i r a . a n d Orius insidiosus for caged tobacco budworm on cot• Bulletin of Entomological Research 71:181 -193. ton treated with chlordimeform sprays. Environmenta l Entomology 5(6):1049-1052. HARDWICK, D.F. 1965. The corn earworm complex. Memoirs of the Entomological Society of Canada 40, LUCKMAN, W.H., and METCALF, R.L. 1974. T h e p e s t Ottawa, Canada. 247 pp. management concept. In Introduction to pest manage• ment (eds W.H. Metcalf and R.L. Luckman). New York, HARTLEY, G.S., and GRAHAM-BRYCE, I.J. USA: Wiley-lnterscience. 1 9 8 0 . Physical principles of pesticide behaviour, volume 1. London, UK: Academic Press LUND, A.E., HOLLINGWORTH, R.M., and SHANK- LAND, D.L. 1979. Chlordimeform: plant protection by a HULL, S.F. 1980. Adult control of Heliothis armigera in sub-lethal noncholinergic action on the central ner v o u s the Sudan. Agricultural Aviation Research Unit prog r e s s system. Pesticides Biochemistry and Physiology 177- report 10/80, Cranfield, UK. 1 7 8 . JOYCE, R.J.V. 1959. The yield response of cotton in the LUTTRELL, R.G., YEARIAN, W.C., and YOUNG, S.Y. Sudan Gezira to DDT spraying. Bulletin of Entomolog i c a l 1979. Laboratory and field studies on the efficacy of Research 50:567-594 selected chemical insecticides-Elcar (B a c u l o v i r u s helio• JOYCE, R.J.V. 1961. Some factors affecting the this) combinations against Heliothis spp. Journal of Eco• n u m b e r s of Empoasca lybica de Berg (Homoptera: Cica- nomic Entomology 72(1 ):57-60 dellidae) infesting cotton in the Sudan Gezira. Bulletin of MACARTHUR, R. 1960. On the relative abundance of Entomological Research 52:191-232. species. American Naturalist 94:25-34. JOYCE, R.J.V. 1978a. Work accomplished in the CIBA- PITTS, D.L, and PIETERS, E.P. 1980. Ovicidal activity GEIGY research programme. In Proceedings, Third of insecticides against tobacco budworm eggs on cot t o n . Seminar on the Strategy for Cotton Pest Control in t h e Journal of Economic Entomology 73(4): 570-572. Sudan. CIBA-GEIGY, Basel, Switzerland. RABB, R.L. 1970. In Concepts of pest management JOYCE, R.J.V. 1978b. Yield response of Gossypium (eds. R.L. Rabb and F.E. Guthrie). Raleigh, NC, USA: N o r t h barbadense in the Sudan Gezira to aerial spraying at ULV Carolina State University Press. rates with Nuvacron 40® . Pages 229-242 i n Proceedings, Third Seminar on the Strategy for Cotton Pest Contr o l in RAINEY, R.C. 1974. Flying insects as targets for ultra- the Sudan. CIBA-GEIGY, Basel, Switzerland. low volume spraying. Pages 20-28 in British Crop Protec• tion Course Monograph 11, Centre for Overseas Pest KNIPLING, E.F. 1972. Entomology and the manage• Research, London, UK. ment of man's environment. In Proceedings, 14th Con• gress of Entomology, Canberra, Australia. RAINEY, R.C. 1976. Flight behaviour and features of the atmospheric environment. Pages 75-112 in Insect flight LAWSON, T.J. 1980a. The population dynamics of Heli- (ed. R.C Rainey). Symposia of the Royal Entomologica l othis armigera in Chaibadan, Thailand, 1979, and the Society of London 7. Oxford, UK: Blackwell. development of a pest control strategy. Agricultura l A v i a - tion Research Unit research report 43/80, Cranfield , UK. RUSSELL-SMITH, N.A. 1975. Distribution and sam• pling of Heliothis armigera (Hb) eggs on cotton in the LAWSON. T.J. 1980b. The toxicity of Nuvacron 40 SCW Sudan Gezira. In Proceedings, Seminar on the Strategy and Curacron 375 ULV to adult Heliothis virescens a n d for Cotton Pest Control in the Sudan Gezira. CIBA-G E I G Y. Spodoptera littoralis. Agricultural Aviation Research Unit Wad Medani, Sudan. progress report 103/80, Cranfield, UK. SCHAEFER, G.S. 1976. Radar observations on insect LAWSON, T.J., and HULL, S.F. 1979. Adult Heliothis flight Pages 157-197 in Insect flight (ed R.C. Rainey). armigera a n d Spodoptera littoralis control trials, Hola, Symposia of the Royal Entomological Society of Lond o n Kenya, 1979. Agricultural Aviation Research Unit pr o - 7. Oxford. UK: Blackwell. gress report 93/79, Cranfield, UK. SMITH, D.B., HOSTETTER, D.L., and IGNOFFO, C M . LAWSON, T.J., TOPPER, C.P., and HULL, S.F. 1978. Formulation and equipment effects on application 1 9 7 9 . A d u l t Heliothis armigera control trials in the Sudan of a viral (Baculovirus heliothis) insecticide. Journal of Gezira, 1979. Agricultural Aviation Research Unit p r o • Economic Entomology 71(5): 814-817. gress report 88/79, Cranfield, UK. SOUTHWOOD, T.R.E. 1974. The dynamics of insect LENTZ, G.L., WATSON, T.F., and CARR, R.V. populations. In Insects, science and society (ed. D. 1974. Dosage-mortality studies on laboratory-reared lar• Pimental) New York, USA: Academic Press. vae of tobacco budworm and the bollworm. Journal of Economic Entomology 67(6)719-720. SPARKS, A.N., JACKSON, R.D., and ALLEN, G.L.

187 1975. Corn earworm: capture of adults in light trap s o n unmanned oil platforms in the Gulf of Mexico (USA). Journal of Economic Entomology 68:431 -432.

STEIN, V.M., SMITH, R.F., BOSCH, R., and HAGEN, K.S. 1 9 5 9 . The integrated pest control concept. Hilgardia 2 9 ( 2 ) : 8 1 .

STADELBACHER, E.A., FARR, R.E., and LASTER, M . L . 1 9 7 2 . Bollworms and tobacco budworms. Mortality of adults exposed to insecticides on cotton. Journa l o f Economic Entomology 65(6):1682-1683.

TAYLOR, L.R., and TAYLOR, R.A.J. 1977. A g g r e g a • tion, migration and population mechanics. Nature 265:415-421.

TAYLOR, L.R., FRENCH, R.A., WORWOOD, I.P., DUPUCH, M.J., and NICKLEN, J. 1980. Synoptic mon• itoring for migrant pests in Great Britain and West e r n Europe. Pages 41 -104 in Rothamsted Experiment Station report for 1980, part 2, Rothamsted, UK.

TOPPER, C.P. 1981. The behaviour and population dynamics of Heliothis armigera (Hb) (Lepidoptera, Noc- tuidae) in the Sudan Gezira. Ph.D. thesis, Cranfiel d Insti• tute of Technology, Bradford, UK.

UK, S., and OUTRAM, I. 1979. Monocrotophos in the extra-floral nectar of cotton after field sprays of N u v a c r o n 40. Agricultural Aviation Research Unit progress report 98/79, Cranfield, UK.

WARE, G.W., ESTESEN, B., and CAHILL, W.P. 1975. Bulletin of Environmental Contamination and Tox• icology 14(5):606-609.

WILKINSON, C.F. 1968. Detoxication of pesticides and the mechanism of synergism. Pages 113-142 in Enzy• matic oxidation of toxicants (ed. E. Hodgson). Rale i g h ,

NC1 USA: North Carolina State University Press.

WILSON, A.G.L. 1974. Resistance of Heliothis armigera to insecticides in the Ord irrigation area of North W e s t e r n Australia. Journal of Economic Entomology 67(2):256- 2 5 8 .

WOLFENBARGER, D.A., and MCGARR, R.L. 1 9 7 0 . The toxicity of methyl parathion, parathion, and monocrotophos applied topically to populations of L e p i - dopteran pests of cotton. Journal of Economic Entomo l • ogy 63 (6)762-764.

WOLFENBARGER, D.A., LUKEFAHR, M.J., and GRA• HAM, H.F. 1971. A field population of bollworms resist• ant to methyl parathion. Journal of Economic Entomolo g y 64(3): 755-756.

188 A Determination of an Economic Injury Level of Heliothis armigera (Hubner) in Sorghum for Southeast Queensland

P.H. Twine and I.R. Kay*

Abstract

A pest density-crop loss relationship lor Heliothis armigera in sorghum (cv Texas 610) in southeast Queensland, Australia, was calculated from a series of trials, using caged heads or natural larval infestations. The loss of 1.56 g per larva derived from this regression has been developed into an economic threshold, and an appropriate sequential sampling program utilizing these values is proposed.

T h e g e n u s Sorghum includes a wide variety of During the latter half of the nineteenth century, grain-bearing plants, ranging in type from tall, tus- many sorghum collections were made by botanists socky grasses to thick, juicy-stemmed sweet travelling in Africa and Asia, most of which found sorghums. The main members of the genus culti• their way to the United States of America, where vated throughout the world are grain sorghums, conditions were much better suited to their growth grown chiefly as a cereal; sweet or fodder sorgh• than in northern and western Europe. In the USA, ums, for green feed or silage; sudangrass for graz• they rapidly gained favor, particularly in the drier ing, hay, and silage; broom millet for brooms and midwestern and southwestern states, where rain• brushware; and, more recently, columbusgrass, fall was often insufficient for successful maize principally for grazing. crops. It is from the USA that many of Queensland's Cultivated sorghum is a crop of great antiquity. It most successful importations have come. is thought to have been grown by the Chinese In Australia, grain sorghum is grown commer• earlier than 2000 B.C., and was grown in Egypt in cially in many areas of Queensland and northwest• Biblical times. The main centers from which it has ern New South Wales, with about 80% of the total spread into modern cultivation are southern Asia, area under the crop in Queensland. Yields of grain Asia Minor, and north and south Africa. In most of sorghum vary considerably from year to year and these countries it has provided a staple cereal for from place to place. Official statistics in recent human food, as well as grain and fodder for anim• years for both New South Wales and Queensland als. It is only in more highly developed modern show that the average yields range from 1.5 to 2.5 communities where wheat, oats, and other cereals metric tons (tonnes)/ha (Table 1). These averages are plentifully available, that sorghum grain has are extremely low when compared with the known been relegated to the position of stock feed. performance of hybrid varieties. This may be a result of shortcomings in fertilizer use and cultural

*Department of Primary Industries, Queensland. Australia. practices.

The array of insect pests attacking sorghum has bee n well d o c u m e n t e d internationally ( Y o u n g a n d Teetes 1977) and locally (Passlow 1973). Passlow (1973) claims that the s o r g h u m m i d g e (Contarinia sorghicola [Coq.]) is, without doubt, the most important of the insect pests attacking sorghum in Q u e e n s l a n d . Although its incidence is s o m e w h a t sporadic, the losses resulting from the attacks have a significant effect on the overall annual production of sorghums. Of the other insects attacking sorghum, the sorghum head caterpillar, Crypto- blabes adoceta (Turn.), the yellow peach moth (Dichocrocis punctiferalis [Guen.]), armyworms (Pseudaletia convecta [Walk.] and Spodoptera spp), cutworms (Agrotis spp), aphids (Rhopalosi- phum maidis [Fitch]), a n d false w i r e w o r m s (Gonocephalum sp) also inflict d a m a g e sporadi• cally. T h e c o r n e a r w o r m (Heliothis armigera [ H u b n e r ] ) was o n c e regarded as falling into this same category, but with the advance of agricultural development in the areas in question, the species is increasingly recognized as a more regular pest of s o r g h u m . Basically, H. armigera is a pest of the fruit or grain development stage, but in sorghum crops it can attack the plant at any stage of growth. Although larvae feeding on the leaves c a n give a very r a g g e d a p p e a r a n c e to a s o r g h u m stand, s u c h d a m a g e is unlikely to c a u s e any real influence on grain yield. Feeding by H. armigera c o m m o n l y o c c u r s on the h e a d but attacks of this kind d e c r e a s e as the grain approaches maturity. Feeding during the soft-grain stages, however, reduced the yield of the individual heads, a n d it is the purpose of this paper to quantify this relationship a n d to discuss the e c o n o m i c impli• cations of the results. Although very few data are available on the e c o n o m i c i m p o r t a n c e of H. armig• era in s o r g h u m , A l c o c k a n d T w i n e (1980) esti• m a t e d the cost of this pest to s o r g h u m production in Q u e e n s l a n d alone at s o m e $4 811 0 0 0 annually. This c o m p r i s e d an estimate of $1 8 4 2 0 0 0 as direct spray a n d spray application costs, together with a residual loss of s o m e $2 9 6 9 000. Obviously, the e c o n o m i c threat of the species to s o r g h u m p r o d u c • tion in Q u e e n s l a n d is quite significant.

Economic Threshold

Although one of the first discussions emphasizing t h e relationship b e t w e e n the density of a pest a n d

190 the potential d a m a g e c a u s e d by the pest was m a d e Table 2. Treatment levels used In caged-head studies by Shotwell (1935), Stern et al. (1959) initiated of the affect of H. armigera on grain sorghum i m m e n s e discussion a n d interest in e c o n o m i c thre• production. sholds and economic injury levels. More recently, c o n c e p t s s u c h as action thresholds (Chant 1966) I n f e s t a t i o n l e v e l a n d control thresholds (Sylvern 1968) have b e e n (larvae/ head) suggested, with Smith (1969) analyzing these var• T r i a l 0 1 2 3 4 5 7 8 1 0 R e p l i c a t e s ious c o n c e p t s a n d c o n c l u d i n g the a d v a n t a g e s of 1 x x x x 3 3 the term "economic" from the practical standpoint. 2 x x x x 3 3 Irrespective of theoretical considerations, the 3 x x x x 6 6 practical implications of the question, "When do we 4 x x x x x x 14 need to control a p e s t ? " have led entomologists to 5 x x x x x x 13 study the effect of pest activity in c r o p s a n d to 6 x x x x x x 15 develop realistic guidelines to assist producers. Stem (1966) discussed three empirical methods a. Glasshouse trial. of establishing economic thresholds, relying on vis• ual estimations of crop loss, while Stone and Pedigo (1972) presented a fourth a p p r o a c h involv• ing costs, marketing, and yield data. The method head) used varied between trials from four to used here basically follows that of Stone a n d seven, with the treatment levels varying from zero Pedigo (1972), thereby allowing for fluctuations in to ten third-instar larvae per head. T h e number of such parameters as market values, insecticide, replicates also varied from 13 to 66, depending on a n d application costs. the availability of uniform heads and larvae. Traditionally, the threshold for Heliothis in T w o of the c a g e d - h e a d trials were c o n d u c t e d in s o r g h u m in Q u e e n s l a n d was estimated to be of the the glasshouse. A summary of the treatment infor• order of four to six larvae per head. This value w a s mation is set out in T a b l e 2. arrived at from practical experience and observa• Larvae were allowed to c o m p l e t e development tion, a n d has provided a realistic basis to date for a n d pupate in the cage. At this stage, the c a g e s pest-management decision-making. More recent w e r e r e m o v e d a n d the pupae counted. T h e d e v e • reviews a n d specific studies of the d a m a g e to loped grain was harvested, threshed, weighed, and s o r g h u m by Heliothis have s u g g e s t e d a s o m e w h a t c o u n t e d at maturity. lower density might be more applicable (Kinzer a n d T h e remaining four trials were c o n d u c t e d using H e n d e r s o n 1968; Wilson 1976; B u c k l e y a n d Burk- natural h e a d infestations in the s a m e variety. hardt 1962). It was in this context that a series of Heads of similar sizes were selected at random and experiments w e r e undertaken from 1970 to 1980 to labeled a c c o r d i n g to the number of larvae present. define m o r e closely the relationship b e t w e e n Heli- (All trials were carried out at a time w h e n the larval othis density a n d resulting d a m a g e . cohort was in the third instar.) As a result, the number of replicates of each larval infestation level was not constant, but rather varied with the overall Methods infestation situation. As with the caged-head trials, the heads were harvested at grain maturity, B e t w e e n 1 9 7 0 a n d 1980, ten trials were under• threshed, a n d the grain weighed a n d c o u n t e d . taken using the c l o s e d - h e a d cultivar, T e x a s 6 1 0 . A summary of the treatment information for these Six of these involved caging artificial larval infesta• trials is set out in Table 3. tions on h e a d s during the grain-maturation stage a n d e x a m i n i n g the resulting d a m a g e a n d yield loss. T h e c a g e s were similar to those u s e d by Kinzer Results a n d H e n d e r s o n (1968). E a c h c a g e w a s s e c u r e d t o the head, and a small quantity of vermiculite was Regression Analyses provided in the bottom as a pupation site. H e a d s were infested with third-instar larvae from either Regression analyses were carried out for s e e d laboratory colonies or natural infestations in t h e weight per h e a d in g r a m s (Y) (corrected to 1 2 % trial area. T h e numbe r of treatments (larvae per moisture content) a n d larval infestation per h e a d

191 decreased head grain yield 3.9 g at harvest. Wilson Table 3. Treatment levels used for field trials on the (1976), o n the other h a n d , f o u n d that e a c h a d d i • effect of H. armigera on grain sorghum production. tional H. armigera larva d e c r e a s e d yield by 5.4 g for cv RS-610 a n d by as m u c h as 8.4 g for cv Pickett. However, these data were generated from mean I n f e s t a t i o n l e v e l weekly larval infestations in large plots (20 m x 100 (larvae/head) Total heads m) rather t h a n from studies of infestations in indi- T r i a l 0 1 2 3 4 5 u s e d vidual heads. For e a c h of the c a g e d trials the n u m b e r of pupae, 7 x x x x x 135 prepupae, or larvae present in the c a g e at the 9 x x x x x x 2 1 3 c o n c l u s i o n of the trial was r e c o r d e d . From these 11 x x x x x x 119 values, it was apparent that the survival of larvae in 12 x x x x 181 the c a g e s varied considerably, a n d several c a u s a l agents a s s o c i a t e d with this p h e n o m e n o n have been identified (Phillips 1931). Therefore, in order to consider m o r e closely the potential d a m a g e (X) for e a c h of the ten trials. T h e critical p a r a m e t e r s caused by individual larvae, grain weights were for these regressions are listed in T a b l e 4, together correlated with a "larval feeding equivalent," which with the values from the pooled regressions for the w a s b a s e d on the m a k e u p of the r e c o v e r e d bodies trials involving cages, natural infestations, and all in e a c h cage. Pupae a n d p r e p u p a e w e r e assigned trials c o m b i n e d . As indicated from the intercept a larval feeding equivalent of 1.0, whereas larval values, t h e s e trials c o v e r e d a w i d e r a n g e of p o t e n • feeding equivalents of 0.6, 0.2, and 0.1 were tial yield situations. T h e within-sets slope for all trial assigned to e a c h sixth-, fifth-, a n d fourth-instar data would indicate that grain-yield loss attributed body recovered respectively. These values were to e a c h additional larva a m o u n t s to s o m e 1.56 g per derived from preliminary dry-matter intake labora• head. tory studies of artificial diet by the six instars of H. This value differs somewhat from previously armigera. T h e s e values also c o m p a r e favorably published values. Kinzer and Henderson (1968) with those of Kinzer a n d H e n d e r s o n (1968) for H. f o u n d f r o m the results of t w o trials that e a c h larva zea.

Table 4. Regression analyses of larval Infestation (larvae par head) and grain weight (g) per head of sorghum.

Correlation

T r i a l dF S l o p e seb coefficient I n t e r c e p t

1 130 - 0 . 1 1 3 0 . 2 4 8 - 0 . 0 3 9 7 2 6 . 1 5 2 130 0 . 0 6 4 0 . 1 3 2 0 . 0 4 2 2 7 . 2 4 3 251 - 2 . 4 7 1 0 . 2 4 0 - 0 . 5 4 0 3 6 1 . 9 9 4 8 2 - 1 . 5 3 8 0 . 1 5 2 - 0 . 7 4 4 5 1 0 . 5 5 5 76 - 0 . 9 7 6 0 . 4 9 4 - 0 . 2 2 0 8 2 1 . 9 1 6 88 - 2 . 4 3 0 1.178 - 0 . 2 1 4 9 7 6 . 0 6 7 133 - 2 . 6 0 3 1.730 - 0 . 1 2 9 4 9 9 . 6 2 8 211 - 0 . 7 3 2 0 . 6 8 9 - 0 . 0 7 2 9 2 6 . 8 1 9 117 - 4 . 3 3 5 1.319 - 0 . 2 9 0 6 1 0 0 . 8 5 10 179 0 . 1 1 9 0 . 7 6 2 0 . 0 1 1 7 3 7 . 0 1

W i t h i n s e t s

C a g e d t r i a l s 7 7 3 - 1 . 5 1 5 0 . 1 4 5 - 0 . 3 5 2 7 Natural infestations 640 - 1 . 9 2 4 0 . 5 7 8 - 0 . 1 3 0 3 A l l t r i a l s 1403 - 1 . 5 6 5 0 . 1 6 9 - 0 . 2 3 9 3

192 potentially at loss equals the cost of control. Or, in Table 5. Regression analyses of larval loading equi- mathematical terms: valent and grain weight (g) per head for caged trials. C x 106 T = P x E Correlation

T r i a l dF S l o p e seb coefficient where T = Threshold as larvae/ha

C = Cost of control ( $ / h a ) 1 130 - 0 . 6 7 4 8 0 . 6 2 5 - 0 . 0 9 4 2 2 130 - 0 . 2 4 8 8 0 . 3 0 6 - 0 . 0 7 1 2 P = Value of commodity ($/tonne) 3 195 - 2 . 2 0 1 3 0 . 4 7 3 - 0 . 3 1 6 1 E = C o n s u m p t i o n per larva (g) 4 8 2 - 3 . 4 2 6 7 0 . 3 3 8 - 0 . 7 4 5 6 5 76 - 1 . 0 9 7 3 0 . 7 7 9 - 0 . 1 5 9 5 S u c h an equation satisfied the situation where 6 88 - 4 . 1 4 0 2 1.119 - 0 . 3 6 6 8 the amount spent on control simply equals the W i t h i n s e t s 7 0 1 - 2 . 1 1 7 8 0 . 2 6 4 - 0 . 2 8 8 9 value of the potential losses. Obviously a farmer will not be willing to a c c e p t this position, as he would n e e d to s e e m o r e value in the potential loss than the outlay for a spray application. Such considera• T h e results of the regression of grain weight (Y) tions involve a benefit:cost ratio. Accordingly, the in grams and larval feeding equivalent (X) for the six formula c a n be a m e n d e d to take this ratio into c a g e d trials are s h o w n in T a b l e 5. account: T h e s e data then indicate the potential loss C x 106 T = x B C c a u s e d by e a c h H. armigera larva in a h e a d to be P x E 2.11 g, in the a b s e n c e of any natural mortality w h e r e BC = Benefit : cost ratio agents. Analysis of the number of H.armigera r e c o • vered from the cages indicate an overall average From previous discussions, it is seen that e a c h mortality of 67%, with values for each trial varying third-instar larva per sorghum head is likely to f r o m 29 to 8 0 % . B e c a u s e of the exclusion of para• reduce yield by 1.56 g. T h e threshold for Heliothis in sites and predators by the cages, this mortality s o r g h u m c a n be derived from: c o u l d be attributed to the cannibalistic habit that C x B C x 106 T = has been well d o c u m e n t e d for Heliothis in s o r g h u m 1.56 x P (Barber 1936; Buckley and Burkhardt 1962.) Using the s o r g h u m h e a d as the ideal sampling unit for Heliothis infestations, it is not unreasonable Economic Considerations to adjust the formula further to:

6 In the establishment of truly meaningful economic C x BC x 10 D = thresholds, proper consideration should be given to 1.56 x P x N a wide s p e c t r u m of direct a n d indirect e c o n o m i c where D = Density of infestation per head variables and social costs of pest control. Headley (1975) has presented an overall review of the e c o • N = Number of heads per hectare n o m i c s of pest m a n a g e m e n t a n d has stressed the complexity of the considerations a n d the n e e d for Because of the number of variables involved, appropriate r e s e a r c h to investigate these. T h e o n e e x a m p l e is prepared. urgent n e e d for s o m e practical guidelines in the For a control cost of $ 2 0 / h a , a benefit: cost ratio adoption of pest-management principles for the of 2 . 1 , value of s o r g h u m at $ 8 0 / t o n n e a n d 200 0 0 0 control of Heliothis in s o r g h u m , however, dictate h e a d s / h a , the threshold would be 1.6 larvae per that at least s o m e d e g r e e of simplicity or first esti• head. mation s h o u l d be taken a n d appropriate thresholds derived. It is in this light that the following thresholds are calculated. Sampling Stern et al. (1959) simply define the injury level as the lowest density that will c a u s e e c o n o m i c d a m • T h e utilization a n d establishment of e c o n o m i c thre• a g e , justifying the cost of artificial control. Alterna• sholds and, often, the selection of control strategies tively, it is the density at w h i c h the value of the grain or tactics will depend on the availability of reliable

193 estimates of pest population densities. S i n c e the 100 collection of data for m a n a g e m e n t d e c i s i o n • m a k i n g differs f r o m that for r e s e a r c h p u r p o s e s in 8 0 that a rapid classification of t h e situation is n e c e s • Spray sary, s o m e practical, unbiased, a n d reliable method of estimating larval densities per hectare is 6 0 required.

Sample Unit N o spray 2 0 Southwood (1966) has suggested that taking many small sample units offers an advantage overtaking only a f e w large o n e s in t h e determination of p o p u • 0 lation parameters. For s o r g h u m , s i n c e most of the 0 2 4 6 8 10 12 Heliothis infestation occurs in the developing head, Number of five-head samples it seems reasonable that this constitutes the ideal sampling unit. T h e unit is easily defined, stable, Figure 1. Sequential sampling plan for Heliothis readily examined, and lends itself to easy conver• spp in sorghum in southeast Queensland, sion to unit areas. Australia.

Dispersion Pattern Obviously the success of such a sequential sampling plan d e p e n d s on the a c c u r a c y of the A detailed k n o w l e d g e of the dispersion pattern of determination of the e c o n o m i c thresholds. Of equal Heliothis in s o r g h u m heads is n e c e s s a r y to indi• i m p o r t a n c e is the n e e d for unbiased sampling of c a t e the intensity of sampling required in order to heads. With a w i d e range of h e a d sizes present in estimate the population p a r a m e t e r s for a set level the field at any o n e time, there is a strong sampling of a c c u r a c y . Infestations of H. armigera in s o r g h u m bias to s a m p l e only those heads "likely" to be were e x a m i n e d in all the trials reported here, a n d infested. To o v e r c o m e this bias, the sampling plan the data s u b j e c t e d to " g o o d n e s s of fit" tests to has been a m e n d e d to use a s a m p l e size of five several standard classes of statistical distributions. consecutive heads. Under these circumstances, As for several insect infestation situations, the neg• given any bias in the selection of o n e h e a d in the ative binomial type of distribution most reasonably sample, the inclusion of the four adjacent heads will d e s c r i b e d the o b s e r v e d data, a n d , using the help minimize the effect of s u c h bias. methods of Bliss and Fisher (1953) a value for k = The major criticism of the practical implementa• 1.8 has been calculated. tion of the sequential sampling m e t h o d is the inordi• nate a m o u n t of time spent in m a k i n g a decision w h e n the infestation approximates the e c o n o m i c Sampling Plan threshold. Onsager (1976) and Sterling (1976) have e v o l v e d a form of truncation of the sampling Pieters (1978) and Sterling and Pieters(1979) have plan to minimize this problem. given a review of the application of the sequential sampling m e t h o d of W a l d (1945) of categorizing pest infestations against economic thresholds in Conclusion pest-management decision-making. Using the value of k f r o m the negative binomial fit, a n d an With a significant trend towards implementing pest- economic injury level of kpo = 1.2 for the level below management programs, particularly in local

w h i c h no action is required, a n d kp1 = 2.0 for the sorghum production, one major deficiency is level a b o v e w h i c h control should be applied, a becoming apparent. This is the lack of reliable sequential sampling plan has been constructed decision-making techniques for Heliothis infesta• using Error I a n d Error II levels of 0.1 by t h e Morris tions. T h e trials undertaken have e n d e a v o r e d to (1954) m e t h o d (Figure 1). establish s o m e k n o w l e d g e of infestation level-

194 damage relationships and to develop this datum SHOTWELL, R.L. 1935. Method for making a grass• into a simple first approximation to an economic hopper survey. Journal of Economic Entomology 28:486- injury level. In association with these trials, studies 491. of the dispersal patterns of H. armigera in sorghum SMITH, R.F. 1969. The importance of economic injury have allowed us to suggest a sequential sampling levels in the development of integrated pest control pro• program as a practical guideline in Heliothis m a n • grams. Qualitas Plantarum et Materiae Vegetabiles (Den agement decision-making in sorghum. Haag). 17:81-92.

SOUTHWOOD, T.R.E. 1966. Ecological methods. Lon• don: Chapman and Hall. 391 pp.

STERLING, W.L. 1976. Sequential sampling plans for References the management of cotton arthropods in south-east Queensland. Australian Journal of Ecology 1:10.

ALCOCK, B., and TWINE, P.H. 1980. The cost of Helio• STERLING, W.L., and PIETERS. E.P. 1979. Sequential this in Queensland crops. Report on Workshop on Biologi• decision sampling. Southern Cooperative Series Bulletin cal Control of Heliothis spp. 23-25 Sept. 1980, 231, College Station, Tex, USA. Toowoomba, Queensland, Australia. STERN, V.M. 1966. Significance of the economic thre• BARBER, G.W. 1936. The cannibalistic habits of the shold in integrated pest control. Proceedings. FAO Sym• corn earworm. Pages 3-18 in U.S. Department of Agricul• posium on Integrated Pest Control 2: 41 -50. ture Bulletin 499, Washington, DC, USA. STERN, V.M., SMITH, R.F., VAN DEN BOSCH, R., and BLISS, C.I., and FISHER, R.A. 1953. Fitting the nega• HAGEN, K.S. 1959. The integration of chemical and tive binomial distribution to biological data and note on the biological control of the spotted alfalfa aphids. Part I. The efficient fitting of the negative binomial. Biometrics 9: integrated control concept. Hilgardia 29: 81 -101. 176-200. STONE, J.D., and PEDIGO, L.P. 1972. Development BUCKLEY, B.R., and BURKHARDT, C.C. 1962. Corn and economic injury level of the green cloverworm on earworm damage and loss in grain sorghum. Journal of soybean in Iowa. Journal of Economic Entomology Economic Entomology 55: 435-439. 65:197-201.

CHANT, D.A. 1966. Integrated control systems Pages SYLVERN, E. 1968. Threshold values in the economics 194-218 in Scientific aspects of pest control. National of insect pest control in agriculture. Statens Vartskyold- Academy of Science, National Resources Council Publi• sanstalt Meddelanden 14: 65-79. cation 1402, Washington, DC, USA. WALD, A. 1945. Sequential tests of statistical hypothe• HEADLEY, J.C. 1975. The economics of pest manage• sis. Annals of Mathematical Statistics 16: 117-186. ment. In Introduction to insect pest management, eds. R.L. Metcalf and W. Luckmann. New York : Wiley. 587 pp. WILSON, A.G.L. 1976. Varietal responses of grain sorghum to infestation by Heliothis armigera. Experimen• KINZER, H.G., and HENDERSON, C.F. 1968. Damage tal Agriculture 12: 257-265. by larvae of the corn earworm to grain sorghum. Journal of Economic Entomology 61: 263-267. YOUNG, W.R., and TEETES, G.L. 1977. Sorghum entomology. Annual Review of Entomology 22: 193-218. MORRIS, R.F. 1954. A sequential sampling technique for spruce budworm egg surveys. Canadian Journal of Zoology 32: 303-313.

ONSAGER, J.A. 1976. The rationale of sequential sam• pling, with emphasis on its use in pest management. U.S. Department of Agriculture, Agricultural Research Service Technical Bulletin 1526, Washington, DC, USA. 19 pp.

PASSLOW, T. 1973. Insect pests of grain sorghum. Queensland Agriculture Journal 99: 620-628.

PHILLIPS, W.J. 1931. The corn earworm as an enemy of field corn in the Eastern States. U.S. Department of Agri• culture Farmers' Bulletin 156, Washington, DC, USA.

PIETERS, E.P. 1978. Bibliography of sequential sam• pling plans for insects. Bulletin of the Entomological Society of America 24: 372-374.

195

The Likely Impact of Synthetic Pyrethroids on Heliothis Management

A. Kohli*

Abstract

An estimated 55 million ha of crops have been treated with pyrethroids since the launch of the first products in 1976 to the end of 1980, when sales reached an estimated value of U.S. $350 million at end-user level. Most of the products have been used against H e l i o t h i s spp, and in situations where this is the main pest, synthetic pyrethroids are expected to acquire a market share in excess of 50%. This paper examines why farmers have found this new group of insecticides so useful and discusses how the chemicals should be used to obtain maximum benefit from their unique properties while avoiding problems that could emerge as a result of the indiscriminate use of a fairly homogeneous group of insecticides on such a large scale.

It has recently been estimated by Wood, MacKen- ables, tobacco, and many others, apparently satis• zie & Co. (ECN 1981) that synthetic pyrethroids fying a wide range of needs under a variety of (SPs) will capture around 2 1 % of the total insecti• climatic and economic conditions. cide market by 1986. The pyrethroid market has Although peasant farmers and growers in indus• grown at an average rate of 55% per year during the trialized countries may have identical expectations last 2 years, as compared with total insecticide of a good insecticide, they may place the main market growth from 1976-1980 of around 14% per emphasis on different aspects of the chemical's year. performance, depending on their type of applica• T h e 3000 tonnes of product sold during 1980 has tion a n d level of sophistication. Equally, a farmer predominantly been used for the control of Helio• may be using insecticides on different crops with a this, much of it on cotton in the USA. different objective or standard of pest control in The very rapid growth in use of SPs, however, mind. For example, he may want to keep his cotton has not been limited to highly developed agricul• virtually pest-free, but may tolerate a certain level ture a n d to cotton; the products have been equally of infestation and damage on less valuable crops well received by unsophisticated farmers in the such as sorghum or pigeonpea. SPs have been tropics for use against Heliothis and other pests on used successfully under a variety of conditions, but cotton, and also on crops such as legumes, veget- the application strategy may have to be modified to exploit those properties of the products most rele•

*Imperial Chemical Industries. PLC, Plant Protection Division, vant to the circumstances. The paper will refer particularly to Heliothis management problems on Surrey. UK.

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India 1 9 7 crops grown by farmers in the tropics and to the strategy, the behavior of the insects, and, not least, SPs permethrin, fenvalerate, cypermethrin, and the behavioral modifications induced by the chemi• deltamethrin. cals. With SPs, as with most other insecticides, it is important to draw a distinction between direct insecticidal activity that can be determined in the Properties that Influence the laboratory and in small plot trials, and performance Performance of Pyrethroids under practical conditions in the natural environment. Against Heliothis SPs yield exciting results in the laboratory, but much of the success in the field is related not so Intrinsic Biological Activity much to their insecticidal effect as to their overall performance, and particularly their potential to Synthetic pyrethroids used in agriculture are insec- increase yields, an indirect benefit that has only ticidally more active by at least one order of mag• been identified during the large-scale use of these nitude than most of the common organophosphates compounds. Some of the mechanisms by which and carbamates, but high activity against insects is SPs protect the plants and by which yields are combined with low mammalian toxicity. Table 1 increased to a greater extent than can be explained compares the activity of some commonly used by outstanding pest kill are not well understood at compounds against Heliothis virescens. Y o u n g e r present and offer scope for further investigation. larvae are generally more susceptible to insecti• Table 2 summarizes the results of trials conducted

cides and under laboratory conditions the LD5 0 for during 1978-1979 to determine the performance of SPs increases approximately by a factor of 2 per Ambush 50 EC (permethrin) in cotton insect control instar. Current products also exhibit a negative under actual field conditions. Trial plots were temperature-activity relationship, and against Heli• selected in 56 locations in five states in India,

othis virescens the LD5 0 increased by 1.5 to 2.5 mainly in irrigated areas, planted with H-4, MCU-5, times between a temperature of 7°C and 27°C and Varalaxmi varieties. All trials were nonrepli- 2 (Whitney and Wettstein 1979). cated, with two plots of 1000 m at each location. In one plot the farmer applied Ambush according to recommendation, on the other plot he used his Spectrum of Activity and Field standard program for comparison. Ambush was Performance applied on threshold, no protocol was fixed for the standard treatment, and cooperator farmers were allowed to exercise their own discretion as to the SPs potentially have a broad spectrum of activity, choice of product, rate, and timing of application. but the biological effect is significantly modified in practice by the rate of application, the application The results shown in Table 2 demonstrate very conclusively that by applying Ambush only as needed, the number of applications can be signifi• cantly reduced, in this case from 12.6 for the best conventional products to 6.9; at the same time, Table 1. Toxicity of soma organophoaphate and yields can be increased by an average of 36%. three pyrethroid Insecticides to third-instar larvae of Scouting played a crucial part in determining the Heliothis virescens by topical application (LDeo ppm). best timing and the longest possible interval between spray rounds. Irrespective of whether

Organophosphates farmers apply sprays on threshold or at fixed inter• vals, lasting and reliable protection of the crop is a Monocrotophos 5 0 0 0 significant advantage, and the relatively long spray Profenophos 5 0 0 intervals associated with SPs is one of their Parathion-methyl 1 2 5 0 strengths. The pyrethroids used in crop protection are more photostable than many of the common Synthetic pyrethroids organophosphates and carbamates. They are all Fenvalerate 6 2 . 5 lipophilic and hence potentially rainfast. Further• P e r m e t h r i n 6 2 - 125 more, good initial control and, in some cases, a Cypermethrin 31 reduction in ovipositing moths allow longer inter-

198 Table 2. Farmer test-use of Ambush In hybrid cottons 1978-79; summary of pooled results (Irrigated cottons: all India).

G u j a r a t Madhya Pradesh T a m i l N a d u Andhra Pradesh K a r n a t a k a A v e r a g e

Observation/Result A m b u s h S t a n d a r d Ambush Standard A m b u s h S t a n d a r d A m b u s h S t a n d a r d A m b u s h S t a n d a r d Ambush Standard

Duration of use (DAS) 6 3 - 1 6 0 6 5 - 1 6 5 63-176 63-176 4 2 - 1 4 2 3 9 - 1 4 5 4 9 - 1 5 9 5 2 - 1 6 0 6 7 - 1 5 3 5 7 - 1 5 3 57-160 57-160 No. of days protected 1 0 0 1 0 0 1 1 3 1 1 3 1 0 0 1 0 0 1 1 0 1 0 6 8 6 8 6 1 0 3 1 0 3 No. of applications 8 . 1 1 2 . 6 6 . 4 1 0 . 0 7 . 1 1 1 . 1 1 7 . 4 1 7 . 6 5 . 5 1 1 . 5 6 . 9 1 2 . 6 Average application 1 3 . 8 7 . 9 1 7 . 7 1 1 . 3 1 4 . 1 9 . 5 1 4 . 9 6 . 1 1 5 . 6 7 . 5 1 4 . 9 8 . 2 i n t e r v a l ( d a y s ) Active ingredient 0 . 8 4 4 2 3 . 9 4 6 0.760 16.912 0 . 7 3 5 1 5 - 7 0 9 0 . 7 6 7 3 8 . 0 0 3 0 . 7 0 4 3 0 . 0 7 5 0.762 24-929 applied (kg/ha)

Cost of insecticides (Rs/ha)a T o t a l c o s t 1 6 8 7 . 7 6 2 2 2 9 . 7 4 1519.20 1551.05 1 4 6 9 . 5 7 1 9 3 6 . 8 6 1 5 3 3 . 5 4 1 8 3 5 . 5 7 1 4 0 7 . 0 0 1 7 8 7 . 5 0 1523.41 1878.14 Cost per application 2 0 8 - 3 6 1 7 6 . 9 6 237.38 155.11 2 0 6 . 9 8 1 7 4 . 4 9 2 0 7 . 2 4 1 0 4 . 2 9 2 5 5 . 8 2 1 5 5 . 4 3 220.79 149.06 Cost per day protection 1 6 . 0 7 2 2 . 3 0 13.44 13.73 1 4 . 7 0 1 8 . 2 7 1 3 . 9 4 1 7 . 0 0 1 6 . 3 6 2 0 . 7 8 14.79 18.23 Saving in cost of insecti• 5 4 1 . 9 8 - 3 1 . 8 5 - 4 6 7 . 2 9 - 3 0 2 . 0 3 - 3 8 0 . 5 0 - 3 5 4 . 7 3 - cides due to Ambush use ( R s / h a ) I n c r e a s e s i n c o s t o f ------i n s e c t i c i d e s d u e t o Ambush use (Rs/ha)

Yield of seed cotton 2 8 0 4 . 0 2 2 2 8 7 . 0 6 2857.30 2170.80 3 1 8 3 . 8 8 2 1 8 3 . 9 7 3 3 4 4 . 6 8 2 4 6 8 . 9 3 2 8 9 3 . 2 5 1 9 5 7 . 2 5 3016.63 2214.60 ( k g / h a ) Increase in yield over 5 1 6 . 9 7 - 6 8 6 . 5 8 - 9 9 4 . 9 1 - 8 7 5 - 7 5 - 9 3 6 . 0 0 - 8 0 2 . 0 3 - standard (kg/ha) Increase in yield over 2 2 . 6 0 - 3 1 . 6 2 - 4 5 . 4 5 - 3 5 . 4 7 - 4 7 . 8 2 - 3 6 . 2 2 - standard (%)

a . Actual price for standard insecticides. For Ambush 50EC an end-user price of Rs.2000/kg ai has been as s u m e d . vals b e c a u s e of the persistence of effect. H o w e v e r , Heliothis s p p t h a n against s o m e of its important there seem to be additional reasons for the lasting predators a n d parasites, a n d they s e e m t o c o m • protection afforded by the SPs. It c a n be o b s e r v e d pare very favorably in this respect with s o m e of the that insects that c o m e into c o n t a c t with residues, most c o m m o n l y used o r g a n o p h o s p h a t e a n d car• e v e n at sublethal concentrations, b e c o m e hyper• bamate insecticides. Plapp and Bull (1978) con• active, b e h a v e abnormally, a n d t e n d not to remain c l u d e d f r o m their studies that of all the insecticides on treated foliage. Ruscoe (1977) calls this effect tested, the SPs as a group proved to be most highly "repellent a n d antifeedant"; H i g h w o o d (1979) pref• selective against the t o b a c c o b u d w o r m . D e l t a m e - ers t h e t e r m "irritancy." This effect c a n directly thrin, for e x a m p l e , w a s 70 times m o r e toxic to H. prolong the protection of the c r o p by preventing virescens than to Chrysopa camea at the LC50 newly h a t c h e d larvae from feeding, particularly at a level and 200 times as toxic at the LC9 0 level. SPs time w h e n r e d u c e d plant g r o w t h or low infestation w e r e also relatively low in toxicity to the parasite pressure makes it possible to space sprays further Campoletis sonorensis. Other researchers (Yehia apart. If insects are not k n o c k e d d o w n following et al. 1979) f o u n d cypermethrin a n d fenvalerate to contact with the spray or the wet deposit, this anti• be the safest c o m p o u n d s against Coccinella unde- feedant effect prevents virtually all further damage cimpunctata L out of 15 c o m m o n l y used cotton f r o m t h e t i m e of application. SPs act mainly through insecticides. Wilkinson et al. (1979) reported f e n • contact, a n d the activity i n d u c e d in insects that valerate a n d permethrin to be significantly less c o m e into c o n t a c t with the spray deposit may toxic to Apanteles marginiventris, a parasitoid, a n d a c c e l e r a t e the poisoning process, m u c h in the three predators of Heliothis spp t h a n the o r g a n o - same way as it puts mobile parasites and predators phosphates sulprophos and profenophos. at a high risk if ordinary, nonselective contact p o i • All this information shows SPs to be promising s o n s are used. insecticides for use in integrated pest management In t h e c a s e of SPs, there is e v i d e n c e that the programs. T h e y are of s u c h low toxicity to most repellent effect may play a role in reducing the predators that at the rates required to control Helio• h a r m d o n e t o w i n g e d parasites a n d pollinators. this, h a r m c a u s e d to beneficial insects t h r o u g h a A l t h o u g h SPs have a broad s p e c t r u m of activity, direct toxic effect should be minimal. Against they have b e e n s h o w n to be m o r e active against mobile parasites, w h e r e the favorable selectivity is

30 Ambush (0.02%) F l i g h t 1 day before t r e a t m e n t

2 5 F l i g h t 1 day after t r e a t m e n t Control ( a v e r a g e of 4 days) Application of water at 10.45 hr 20 Application of Ambush during the flight activity 15

0 9 10 11 12 13 14 1 5 16 17

T i m e

Figure 1. Repellent effect of Ambush compared with flight activity before and after the treatment day and with the average value for 4 days.

2 0 0 slightly less pronounced, the repellent effect can depressing effect exerted by conventional further enhance the safety of SPs. Figure 1 shows chemicals. the results of detailed work carried out with honey - bees in the flight-tent by Gerig (1979). Ambush repelled bees almost completely for several hours, Use of Synthetic Pyrethroids for and bees did not visit the treated plants to any Protection Against Heliothis Attack appreciable extent during the day of treatment. Returning to the subject of crop yields, the effec• Synthetic pyrethroids are very versatile and can be tive protection provided can in many cases, pass successfully used under varying conditions. as an explanation for the yield increases obtained. Because of their high insecticidal activity, it is But experience with pyrethroids has also shown tempting to use them as insecticides have tradi• that there are often yield increases in conditions tionally been used—to eradicate established infes• where pest control on pyrethroid-treated and con• tations or as a preventive spray applied more or ventionally treated areas is very similar. This is one less according to a schedule, with the objective of aspect that has not yet been fully elucidated, but keeping the crop pest-free. the possibility of growth-regulant effects on plants Most of the SPs used against Heliothis on field cannot be excluded. It has often been observed crops in the tropics have been used in this way. that crops treated with pyrethroids, particularly Experience, particularly in cotton, has shown that such crops as vegetables and cotton, which SP use follows a certain pattern. During the period receive several sprays, look healthier and lusher following the launch of the first products, farmers and often mature earlier and more uniformly than often treat them as superior insecticides and apply crops treated with conventional chemicals. them only when the infestation is building up and In a plant-growth test on glasshouse-grown conventional products are no longer giving ade• tomatoes that were treated five times at 5-day quate control. Often they will also use pyrethroids intervals, with three rates of Cymbush 10 EC, as a component of a tank mixture. As more pro• Ambush 50 EC, and Docis 2.5 EC, the SP-treated ducts enter the market, price competition plants were on average 2.1 cm or 15% taller 25 increases, and farmers recognize their effect on days from the start than the plants sprayed with yield and early maturity in addition to their out• water. standing insecticidal activity, many will use SPs Table 3 summarizes the results of a trial carried almost exclusively, with generally very satisfactory out by Imperial Chemical Industries (ICI) in the results. USA, in which the damage levels between plots Unfortunately, the high level of efficacy against treated with Cymbush at 28 g ai/ha and the stand• Heliothis, the reliable performance of the product ard were comparable, but in which the plots treated against this pest, and the relatively low cost of SPs with Cymbush yielded 29% more. However, it do lead farmers to neglect other aspects of pest remains open to discussion whether this and many management. Whilst application techniques have similar results can be explained by a yield- generally improved in connection with SP use,

Table 3. Control of cotton bollworm (Heliothis zea) and tobacco budworm (H. virescens) on cotton with full-season program (7-day schedule), USA.

Rate D a m a g e d L i n t Y i e l d T r e a t m e n t ( g a i / h a ) squares (%) ( k g / h a )

Cypermethrin 2 8 13 402 Cypermethrin 56 9 6 0 9 Methyl-parathion 1 1 2 0 15 311 + t o x a p h e n e C o n t r o l 2 5 6 7

201 most growers still seem reluctant to use scouting to tial of SPs to the fullest possible extent may be apply the products as needed on their more valu• rewarded with a yield increase. able crops. Most prefer to spray when the time seems right or when neighbors begin their treatments. Irraddition, Obtaining Maximum Benefits from SPs little attention has been paid to the fact that SPs do not control mites, and, depending on the method of Suggestions will now be made as to how the maxi• application, may not adequately control some of mum benefit can be obtained from the unique prop• the more hidden sucking insects. In more mature erties of the SPs, using the lowest possible amount markets such as Thailand, where SPs have been of active ingredient and with the least impact on the the main insecticides used over several seasons, it e c o s y s t e m . has become apparent that SPs will not be a pana• Given the decreasing susceptibility of older cea for all types of pest attack, and their indiscrimi• caterpillars, accentuated by usually high ambient nate use will allow pests that they do not control temperatures, it is important to apply the SPs early. well to gain in importance. Furthermore, it must be Not only are young larvae more susceptible, but assumed that SPs as a weapon against Heliothis first and second instars are also more exposed will be blunted prematurely if they are used for the than later instars. On cotton, more than 95% can be control of pests for which they are not particularly found on emerging leaves at the branch tips and suitable. small buds (Mabett et al. 1980), and they wander Considering the savings in chemical and expen• about on the plant a great deal until they find a diture that farmers could make in return for the little suitable feeding site (Pearson 1958). extra time needed to monitor pest infestation levels, In order to decide whether the infestation by a it is difficult to understand why reality is still so far pest has reached the economic threshold and a removed from the ideal. No doubt a great deal of spray is required, regular scouting is essential. On work has already been done by the agricultural crops where Heliothis or another lepidopterous extension services, the scientific community, and pest is the main target, SPs should not be used until commercial companies, and there are isolated these pests have reached the economic threshold, signs of farmers adopting more sophisticated pest- which, of course, will be different for different c r o p s control strategies. The large majority of farmers, and in different economic situations. On cotton, however, are not yet ready or able to follow pest- where early bollworms usually cause little eco• control recommendations based on principles of nomic damage, it will not normally be necessary to integrated pest management. apply the products before the onset of the main Farmers growing cash crops are normally not flowering phase. prepared to take risks and are often willing to take Up to this time it is best to avoid insecticidal out insurance in the form of early and additional treatments or to use soil-applied or selective applications of insecticides. From a technical point chemicals, a practice that will help to conserve of view this may seem wasteful, but perhaps from beneficial insects. They can assist in delaying the their position it is logical. The farmers' livelihood is onset and reducing the intensity of mid-season at stake, and a lower but secure income may be Heliothis attack. preferable to a potentially higher reward, with the When economic damage is expected, for exam• risk of severe losses from time to time. The farmers' ple, on cotton from about day 50 onwards, the crop present strategy may be the one best suited to their should be scouted at regular intervals (for high- requirements and capabilities, given the social value crops about twice a week). Numbers of black structure, lack of education, dependence on illiter• eggs or larvae may be used as the threshold. In ate laborers, unpredictable weather, inefficient areas and on crops where egg parasitism is high spray equipment, and insecticides that are more and infestaton pressure low or moderate, the effective in preventing Heliothis infestation than in number of larvae may give a more reliable indica• cleaning up the crop once the pest is well tion than the eggs. Eggs, on the other hand, give entrenched. This reality cannot be ignored by a more advance warning and should be counted if commercial company, and recommendations for infestation pressure is high and the question is the use of SPs have generally taken this situation when—rather than whether—to spray. into account. It is reassuring to know that farmers If infestation is high and the growth of the plants who are not able to exploit the pest-control poten- rapid, spray applications should be made at short

2 0 2 intervals to protect the n e w growth, w h i c h may throid. W h e n using low rates, w h i c h are selectively otherwise be attacked by larvae repelled f r o m effective against Heliothis but leave predators a n d treated older foliage. A low rate/short interval stra• parasites largely unharmed, it is important to apply tegy is also preferred to the high rate/longer inter• the spray w h e n the pest is still vulnerable. T h e level val option b e c a u s e it will give better spray of control aimed for should be related to the e c o • distribution a n d increase the c h a n c e of obtaining nomic threshold a n d the lowest possible rate giving direct spray impingement on adults, larvae, a n d the desired level of control should be c h o s e n to eggs. avoid unnecessary toxic effects on beneficials, but If the e c o n o m i c threshold is low a n d the infesta• perhaps more important in the c a s e of SPs, the tion pressure high, as is often the c a s e in cotton, complete destruction of the prey. then beneficial insects can play only a small role, If insecticide application based on the results of certainly o n c e the spray program has started. For regular scouting is not practical in high-value crops these reasons, SPs should not be used to c l e a n up s u c h as irrigated cotton, it may seem even less established infestations a n d in the a b s e n c e of any likely that it would be a c c e p t a b l e in less valuable other insecticide that is suitable for s u c h a use, it is crops. It is true that under normal c i r c u m s t a n c e s not advisable to c h o o s e an artifically high threshold sophisticated scouting techniques are not in the hope that parasites and predators might employed, and farmers are unlikely to link infesta• eventually prevail. The high-threshold option is fre• tion levels with the abundance of beneficial insects. quently a n d quite successfully e x e r c i s e d in C h i n a , T h e r e are at least two reasons for w h i c h growers but the conditions differ from those in most other follow a more integrated approach to pest m a n a g e • countries in that the cultivation a n d the pest-control ment on semi-intensive crops, albeit u n c o n • program for a large area are c o o r d i n a t e d centrally, sciously. They are prepared to accept a certain no really effective insecticides are available to level of infestation a n d d a m a g e before resorting to date, a n d manual labor c a n be used to collect insecticide application, and secondly—also caterpillars in an e m e r g e n c y in order to bring the related to the e c o n o m i c s of the c r o p — t h e y are less situation under control. likely to overdose in an attempt to eradicate the If infestation pressure f r o m Heliothis is continu• pests. Although the amount of SPs used on semi- ous and high a n d the c r o p has to be sprayed at intensive crops for the control of Heliothis will be regular intervals, it is best to use SPs for several small c o m p a r e d with the p r o g r a m m e d use on cot• sprays in s u c c e s s i o n a n d not to alternate with ton, the use of additional, nonchemical elements of insecticides belonging to another group, unless pest m a n a g e m e n t in these crops and crops not scouting results indicate an a b u n d a n c e of pests treated with the products at all will be an essential that are not adequately controlled by SPs. This prerequisite for the continual intensive use of SPs strategy fully exploits the residual properties of the on cotton and other crops with low e c o n o m i c c o m p o u n d s , with the old deposit contributing to the thresholds. insecticidal level. Furthermore, it is believed that short-term rotation with c o m p o u n d s belonging to different groups has a similar effect as random tank mixtures a n d c o u l d accelerate the selection of Conclusion strains of insects with broad-based resistance, i.e., a m e c h a n i s m of simultaneous resistance to insec• In conclusion, two types of use for SPs against ticides belonging to different groups of chemicals. Heliothis c a n be distinguished. The products are A third reason for exclusive application of SPs dur• suitable for multiple application on high-value c a s h ing the main period of fruit formation a n d g r o w t h — crops such as high-yielding cotton and certain on cotton often b e t w e e n about 50 a n d 110 days vegetables, on w h i c h only a little or no pest d a m a g e after sowing—is that conventional insecticides c a n be tolerated and where the scope for beneficial t e n d to c o u n t e r a c t the SPs' effect on yield. insects during the main growing period is very For crops in which higher economic thresholds limited. In these crops, SPs, applied either a c c o r d • are a c c e p t a b l e , a different strategy c a n be ing to need o r — m o r e likely in the c a s e of the aver• pursued, a n d integration of SPs a n d beneficial age grower—at more or less fixed intervals, provide insects becomes a practical possibility. Ideally, the c r o p with outstanding protection f r o m Heliothis scouting should be used to determine whether a n d spp attack and encourage early maturity (cotton) w h e n there is a n e e d for the application of a pyre- a n d higher yields.

2 0 3 In c r o p s needing less c o m p l e t e protection, as YEHIA, A.I., EL-SAYED, A.M.K., N E G M , A.A., HUS• m a y be the c a s e for rainfed cotton, legumes, SEIN, M.H., and EL-SEBAE, A.H. 1979. The relative s o r g h u m , sunflower, etc., SPs c a n be used as part toxicity of certain insecticides to Spodoptera littoralis and of an integrated control p r o g r a m in w h i c h their low Coccinella undecimpunctata. International Pest Control July/August: 79-82. toxicity to predators a n d their irritant effect on mobile parasites and pollinators are of major importance.

Acknowledgments

I thank my c o l l e a g u e s in t h e Plant Protection Div- ison a n d T h e Alkali a n d C h e m i c a l Corporation of India Ltd. for their cooperation, and in particular Mr. S.R. N e n e of A C C I w h o kindly provided s o m e of the data.

References

ECN (European Chemical News), 5 Aug 1981:5.

GERIG, L. 1979. The toxicity of synthetic pyrethroids to foraging bees. Swiss Federal Research Institute, Liebe- feld, Berne, Switzerland.

H I G H W O O D , D.P. 1979. Some indirect benefits of the use of pyrethroid insecticides. Pages 361 -369 in Pro• ceedings, British Crop Protection Conference, Pests and Diseases. Vol. 2. 19-22 Nov 1979, Brighton, UK.

MABETT, T.H., DAREEPAT, P., and NACHAPONG, M. 1980. Behavior studies on Heliothis armigera and their application to scouting techniques for cotton in Thai• land. Tropical Pest Management 26(3): 268-273.

PEARSON, E.O. 1958. The insect pests of cotton in tropical Africa. Commonwealth Agricultural Bureau, Lon• don, UK.

PLAPP, F.W., and BULL, D.L. 1978. Toxicity and selec• tivity of some insecticides to Chrysopa carnea as preda• tor of the Tobacco Budworm. Environmental Entomology 7: 431 -434.

RUSCOE, C.N.E. 1977. The new NRDC pyrethroids as agricultural insecticides. Pesticide Science 8: 236-242.

WHITNEY, W.K., and WETTSTEIN, K. 1979. AC 222, 705, a new pyrethroid insecticide: performance against crop pests. Pages 387-394 in Proceedings, British Crop Protection Conference, Pests and Diseases, Vol.2.19-22 Nov. 1979, Brighton, UK.

WILKINSON, J.D., BIEVER, K.O., and IGNOFFO, C M . 1979. Synthetic pyrethroid and organophosphate insecticides against the parasitoid Apanteles marginiventris and the predators Geocoris punctipes, Hippodamia convergens and Podisus maculiventris, Journal of Eco• nomic Entomology. 4:473-475.

2 0 4 Discussion—Session 4

T h e very large populations of Heliothis larvae on chemicals were used for the control of a single s o r g h u m a n d the large n u m b e r s of e g g s on cotton pest—Heliothis. This was temporarily successful, reported by T w i n e c a u s e d s o m e surprise. He but later failed because other pest problems, explained that a wide array of host crops in that including whitefly and Spodoptera littoralis, d e v e - area encourages a large buildup of the local Helio- lopd in the area covered by the new strategy. In this populations towards the e n d of the s u m m e r reply, Dr. J o y c e defended the c h a n g e d strategy, season. Although there was an unusually high d e n - which involved the use of monocrotophos to kill sity of e g g s on the cotton, a d e q u a t e control of this Heliothis moths, their y o u n g larvae, a n d whitefly. pest w a s obtained by the application of synthetic He stated that this pesticide had a half-life of 24 pyrethroid sprays. hours w h e n applied in the Gezira, and was prefera• Dr. Saxena reported that significant phytotonic ble to persistent pesticides s u c h as D D T , w h i c h effects had been recorded w h e n c h i c k p e a s were had been recorded to have led to a doubling of treated with synthetic pyrethroids for H. armigera whitefly populations at 30 days after spraying. control at Delhi. He a s k e d whether s u c h effects The new recommended strategy gave excellent had been recorded elsewhere. He also reported control of Heliothis and maintained whitefly at n o n - that economic threshold levels for Heliothis on d a m a g i n g levels on cotton for the first 100 to 120 c h i c k p e a have been determined in India a n d that days after planting. It was recommended that similar determinations are now in progress for spraying should c e a s e after that date, for experi• pigeonpea. Dr. Kohli confirmed that yield effects ments had shown that elimination of leaf-feeding following synthetic pyrethroid use have been amply pests after the cotton was more than 110 days old d o c u m e n t e d , but the c a u s e s of s u c h effects are not gave no yield benefit. Also, there was an immigra• easily identified. He explained that yield differences tion of beneficial insects into the cotton at this time could be a result of m a n y factors, including photo- from groundnut and sorghum that were completing toxicity of the pesticides used in the c h e c k plots their development, and from weeds in the crops a n d differential control of pests that were not the and fallows that were drying up. subject of investigation a n d so were not recorded. Whitefly was not a new problem in the Gezira. He w o u l d w e l c o m e an investigation by i n d e p e n d • C o w l a n d had recorded whitefly problems in 1933- ent r e s e a r c h workers on the effect of synthetic 34. In s o m e years whitefly had built up in early- pyrethroids on c r o p productivity. In response to Dr. season outbreaks that reduced cotton yields. Saxena's c o n c e r n about the toxic residues left on Late-season reductions of whitefly populations had legume a n d oilseed crops at harvest after treat• been c a u s e d not by natural enemies but by the ment with persistent pesticides for the control of collapse of their environment—i.e., the senes• Heliothis larvae, Dr. J o y c e c o m m e n t e d that he c e n c e of the leaves on w h i c h they fed a n d this would m u c h prefer that the target for control m e a • senescence was hastened by jassid attacks. In sures be the moths a n d not the larvae. He said that recent years whitefly has been kept below the level the m o t h s could be killed either by direct contact of economic injury by the new strategy during the with very light doses of pyrethroids that woul d vegetative stage of the crop. Late-season pesticide a c c u m u l a t e during their flight from plant to plant, or use has exacerbated the whitefly problem by by s t o m a c h poisons used in baits. C h a n g i n g the reducing jassids and thus delaying leaf senes• target from the larvae to the moths c o u l d result in c e n c e . In addition, the policy of watering Acala r e d u c e d contamination risks. cotton until picking, a n d so further delaying leaf There was a lively discussion concerning the s e n e s c e n c e , has also increased the whitefly prob• pest problems in the S u d a n Gezira. Dr. Galal H a m i d lem. T h e S. littoralis problem appeared to have O s m a n c o n s i d e r e d that s o m e of the problems had been associated with the increased areas of been caused by changing the pre-1969 policy of groundnut grown in the Gezira in recent years. Dr. using pesticides k n o w n to be soft to natural e n e • Galal H a m i d O s m a n could not a c c e p t this view of mies, a n d alternating these to avoid the develop• the events. ment of resistance. In the n e w strategy, two

2 0 5

Session 5

Host-Plant Heliothis Interactions and Resistance Screening

Chairman: W. Reed Rapporteurs: P.W. Amin Cochairman: A.C. Bartlett S.S. Lateef

The Importance of Heliothis-Crop Interactions In the Management of the Pest

B.R. Wiseman*

Abstract

The importance and use of the resistant crop cultivar in an integrated pest-management sys• tem are reviewed. Today, more than 100 varieties or inbreds, which carry resistance to more than 25 insect species, have been released. Research on plants resistant to insects has been estimated to give about $300 return for each $1 invested. The use of the resistant crop cultivar has been established as a primary method of control of the insect or damage, and as an adjunct to other integrated pest-management components. Examples of Heliothis -crop interactions in relation to the mechanisms of resistance are illustrated.

A knowledge of pest-crop interactions in the man- reported that the most effective and ideal method of agement of insect pests is of paramount impor- combating insects that attack plants was to grow tance. The development and use of a particular insect-resistant varieties; he further showed the cultivar is the base from which all management value of research on and development of resistant strategies must arise. If the crop cultivar is suscept• plants to be about $300 return for each $1 invested. ible, i.e., one that is readily attacked and damaged Dahms (1972b) showed that more than 100 varie- by the pest, then efforts must concentrate on cer• ties or inbreds of crop plants have been released, tain other control tactics. However, if the crop cu l • carrying resistance factors to more than 25 insect tivar is resistant, i.e., it is inherently less damaged or species. Today, probably more than 300 cultivars, less infested than comparison cultivars (Painter resistant to more than 40 insect species or bio- 1951), then the use of the resistant cultivar should types, have been developed. Over 800 literature become the base of all present components used citations related to plant resistance to Heliolhis spp in the management of the pest. were reported in the recent bibliography published by the soybean scientists Kogan et al. (1978). Of The Value of Host-Plant Resistance these, 470 were on general plant resistance, 286 were related to resistance in corn, 122 in cotton, 19 Holcomb (1970) stated that several United States in soybeans, 14 in tobacco, 9 in vegetables, and 11 Department of Agriculture (USDA) officials have in other crops. referred to the use of crops that are highly resistant or even moderately resistant to insect attack as the most successful and least heralded of all the natu• The Uses of Host-Plant Resistance ral methods of insect control. Luginbill (1969) The use of resistant cultivars usually occurs in one of two ways: (1) as a primary method of control and *U.S. Department of Agriculture, Agricultural Research Service, Southern Grain Insects Research Laboratory, Tifton, Ga, USA. (2) as an adjunct to other control components. The

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. 2 0 9 development and use of the resistant cultivar dis• examples exist where research has demonstrated courages the release of susceptible ones. Adkis• that certain plant characters reduced Heliothis spp son and Dyck (1980) stated that the integrated densities (Lukefahr et al. 1971; Wiseman et al. system is designed to suppress pest numbers 1978a). Lukefahr et al. (1971) suggested that the below crop-damaging levels, not to replace chemi• use of glabrous cottons, with the resultant cal pesticides. They further stated that a resistant decrease in Heliothis oviposition, could delay the variety provides a foundation on which to build an need for insecticides and might permit other bio• integrated control system. logical factors to be utilized more effectively. It is widely accepted that full-season corn HPR as a Primary Method of Control hybrids with husks that extend beyond the ear are utilized in the southern USA as a means of limiting corn earworm, Heliothis zea (Boddie), losses. Many examples exist where the use of resistant Because these corn hybrids show tolerance to the cultivars is the primary method of suppressing corn earworm rather than resistance, the insect insect densities or reducing pest damage. HPR population is not suppressed (Wiseman et al. was historically sought in areas and for crops 1972); in fact, the tolerant corn hybrids could very where plant resistance was the only possible plant- well be the major contributing factor to the large protection method (Horber 1972); for example, population buildups in certain areas of the southern grape stocks resistant to Phylloxera sp were first U.S. Gross et al. (1976) reported that even whorl- used in 1870. Wheats resistant to Hessian fly, stage corn could be a primary contributor to the Mayetiola destructor (Say), and wheat stem sawfly, early-season buildup of H. zea. Cephas cinctus Norton, are present-day examples; the planting of some 8.6 million hectares of corn The use of resistant cultivars is also compatible hybrids resistant to European corn borer, Ostrinia with insecticidal control. For many years corn, nubilalis (H'ubner), is another example (Schalk and especially sweet corn, could not be grown eco• Ratcliffe1976). nomically in the southern USA until moderate corn earworm resistance was introduced into the The use of resistant cultivars as a primary control hybrids (Maxwell 1972). McMillian et al. (1972) and measure in historical cases has precluded the use Wiseman et al. (1973) demonstrated the use of a of other control components. The results have resistant (tolerant) sweet corn hybrid plus insecti• been specific, cumulative, and persistent (Painter cide to reduce losses from the earworm (Fig.1). A 1966; Luginbill and Knipling 1969). In certain reduction of about 7.5 kg/ha of insecticides was cases, the insect was eradicated from some locali• realized through a reduction in both rate and ties (Painter 1966). Adkisson and Dyck (1980) number of applications (Table 1). The use of stated that reduction in pest numbers achieved sorghum hybrids resistant to greenbug, Schizaphis through the use of resistant plants is constant, graminum (Rondani) biotype C, permitted the use cumulative, and practically without cost to the of extremely low dosage rates of pesticides (Cate grower. et al. 1973). Low pesticide rates also preserved natural biological control agents and prevented HPR as an Adjunct to Other Control resurgence of the greenbug (Teetes 1980). Measures Refai et al. (1979) reported that Heliothis armigera (H'ubner), a polyphagous insect, was thought to The use of the highly resistant crop cultivar in most have different levels of susceptibility to insecticides cases eliminates the need of most other control as a result of feeding on different host plants. In components. However, with lesser degrees of res• general, the larvae fed on tomato fruits were the istance, other control components must be used. most sensitive to insecticides; those fed on castor This system is of great benefit to the grower and bean leaves and cotton bolls were moderately sus• may enhance the use of other control components ceptible; and those fed on corn ears showed the such as insecticides, predators and parasites, least susceptibility to insecticides. Because of this pathogens, and cultural methods. phenomenon of differential susceptibility, it is po s • There are no clear examples where resistant sible that the use of resistant (antibiosis) varieties crop cultivars that are hosts to Heliothis spp h a v e within a crop species could render the pest even been planted on farms as a primary insect-control more susceptible to insecticides. Therefore, it fol• measure in suppressing this pest. But several lows that the use of several resistant crop species

2 1 0 100 ( N a t u r a l ) on a polyphagous insect s u c h as Heliothis s p p Res. hyb.+ chem. should result in dramatic suppression of the pest. In a closely related area of research, the use of 9 0 (Artificial) c h e m i c a l plant-growth suppressants in cotton for Sus. hyb.+ chem. Res. hyb. + chem reducing late-season Heliothis spp feeding sites was demonstrated by T h o m a s et al. (1979). T h e y 8 8 0 found in 1978 that larval feeding sites were R e s i s t a n t hybrid R e s i s t a n t hybrid r e d u c e d on an average of 8 5 % a n d that larval a n d egg populations were r e d u c e d on an average of 7 0 6 4 % at five locations. Crop terminators in cotton, s u c h as the plant-growth suppressants, could 48 c o m p l e m e n t the use of resistant varieties or other 56 30 Sus. hyb. + chem. control components in eliminating Heliothis estab• lishment on late-season foliage and fruit, and con• sequently reduce contributions to the over- S u s c e p t i b l e hybrid 20 wintering populations. 27 T h e demonstration of the combination of the res• istant cultivar with the use of predator-parasites 10 has been difficult, even though the resistant plants are extremely compatible b e c a u s e resistant cultiv- S u s c e p t i b l e h y b r i d ars do not greatly affect the natural enemies of the 0 pest species. Wiseman et al. (1976) found that populations of Orius insidiosus (Say), a predator on Figure 1. Percentage damage-free ears result- H. zea larvae, were higher on the tolerant corn ing from combinations of resistant or suscepti- hybrids than on the susceptible hybrids, an indica• ble sweet corn hybrids with insecticide and tion of the compatibility of the resistance a n d the natural or artificial infestation of insects 1970. predator. Where a high level of resistance signifi• (Source:McMillian et al. 1972.) cantly reduces the damaging insect population, the effectiveness of the predator or parasite b e c o m e s even more difficult to measure, since the host is being quickly reduced, thus preventing parasite Table 1. Percentage earworm damage-free ears of a buildup. T h e use of a tolerant or moderately antibio• resistant and susceptible sweet corn hybrid after tic cultivar, however, allows full use of the predator- receiving varying numbers of applications of 1.1 parasite components of an integrated system. kg/ha of Gardona® WDL4, Tlfton, Ga, USA. Teetes (1976) and W i s e m a n a n d Morrison (1981) indicated that the development of open- a Mean % damage-free ears headed, partially resistant sorghum hybrids provide S t o w e l l ' s a favorable environment for increased predation N o . o f 471-U6 X 81-1 Evergreen a n d parasitism of H. zea. The effect of resistance applications (resistant) (susceptible) plus biological control is usually not fully appre• ciated until one observes a compact sorghum head

7 74.4 a 47.3 c loaded with H. zea larvae a n d a c c o m p a n y i n g 5 64.5 b 35.0 d molds. 3 6 0 . 1 bc 2 4 . 2 e Since interactions that involve the Heliothis- 2 52.1 c 23.4 e resistant plant and predators or parasites have not 1 50.3 c 10.3 f been published, the first demonstration of the inter• 0 29.7 de 6.6 f actions of greenbug-resistant barley a n d the par• asite Lysiphlebus testaceipes (Cresson) on the Source : Wiseman et al. (1973). greenbug (Starks et al. 1972) is s h o w n as an e x a m • a . Values followed by the same letter are ple. They showed that a resistant variety of barley not significantly different (P=0.05). c o m p l e m e n t e d the activity of the parasite in r e d u c • Percentage based on ratings of 40 ears/ ing d a m a g e to plants a n d production of g r e e n b u g s r e p l i c a t e . (Figs. 2 and 3). Starks et al. (1974) later showed the

211 2 0 0 No parasite

No parasite 100

P a r a s i t e P a r a s i t e

0 Infested with 3 aphids/plant

2 0 0 No parasite

No parasite

100

P a r a s i t e P a r a s i t e

0 Infested with 6 aphids/plant

2 0 0 No parasite No parasite

100

P a r a s i t e P a r a s i t e

0 0 1 2 3 4 0 1 2 3 4 Weeks after infestation Weeks after infestation Infested with 12 aphids/plant C v Will b a r l e y Cv Rogers barley

Figure 2. Increase of greenbugs In the absence and presence of one female parasite caged on greenbug-resistant (Will) and susceptible (Rogers) barley; three replications (Source: Starks et al. 1972.)

2 1 2 2 4 0

Infested with: 3 aphids and 1 parasite

2 1 0 6 aphids and 1 parasite

12 aphids and 1 parasite

p l a n t s d e a d

1 8 0

1 5 0

1 2 0

9 0

6 0

3 0

0 0 1 2 3 4 1 2 3 4 Weeks after infestation Cv Will Weeks after infestation Cv Rogers Figure 3. Production of L. testaceipes mummies on greenbug-resistant (Will) and susceptible (Rogers) barley misted with three populations of greenbugs; three replications (Source: Starks et al. 1972.)

2 1 3 interactions involving a resistant and susceptible agroecosystem. This was because the greenbug sorghum with the greenbug and the same parasite could attain adequate numbers on these cultivars (Fig. 4). The increase in greenbug abundance was to maintain beneficial insect populations. Conse• much more pronounced on the susceptible quently, the beneficials could maintain greenbug sorghum plus parasites than on the resistant density below the e c o n o m i c injury level. sorghum plus parasites. However, the value of The use of entomopathogenic bacterium, fun• greenbug-tolerant sorghum in combination with gus, and virus for control of H. zea on soybeans was natural parasites and predators was reported by reported by Ignoffo et al. (1978), where they Teetes (1976). He reported that the principal showed that larval numbers could be reduced by mechanism of resistance to the greenbug in the 92 to 100% with a virus, 69 to 96% with a bacterium, s o r g h u m s released by T e x a s A & M University at and 19 to 77% with a fungus. Mohamed et al. (1978) that time was tolerance. The economic injury level demonstrated in cage tests the use of Nomuraea was raised with little or no disruption of the rileyi (Farl.) Samson on cultivar Dixie Queen sweet

1 0 0 0 0 1 0 0 0 0

9 0 0 0 9 0 0 0 Greenbugs only

Greenbugs + low 8 0 0 0 parasitoids 8 0 0 0 Greenbugs + high parasitoids 7 0 0 0 ■7000

6 0 0 0 ■6000

5 0 0 0 •5000

4 0 0 0 4 0 0 0

3 0 0 0 3 0 0 0

2 0 0 0 ■2000

1000 1000

2 3 4 5 6 2 3 4 5 6 2 3 4 5 6 2 3 4 5 6 Resistant sorghum Susceptible sorghum Resistant sorghum Susceptible sorghum Greenbugs/plant Mummies/plant W e e k s

Figure 4. The relationship between various levels of parasitoids and greenbug populations on resistant and susceptible sorghum (Source: Starks et al. 1974.)

2 1 4 corn for control of the corn earworm. Mortality response decreased in the following order: corn among fourth-instar larvae was 95% in early > tobacco > soybeans > cotton, and preference summer and 88% in mid and late summer. All ears for corn, soybeans, and cotton was positively received some damage, but damage on the treated correlated with an increase in plant maturity, the ears was significantly lower. The use of resistant peak being at flowering. After flowering, the prefer• varieties in both of these cases would complement ence decreases with senescence of the plant. Pre- the use of insect pathogens, especially when more torius (1976) reported somewhat different results time is required to attain control of the pest. Toler• with H. armigera when he found that, based on net ant corns should permit the insect to feed longer in reproductive rates, the best food was cotton buds the presence of the pathogen, where the antibiotic and leaves, followed by groundnut leaves, sun• type of resistance should render the insect more flower heads, green beans, rose petals, potato susceptible to the insect pathogens. Fernandez et leaves, lucerne leaves, grain sorghum panicles, al. (1969) tested the combinations of resistant cot• young maize cobs, and tomato leaves. Larvae did ton (glabrous and nectariless) with a nuclear not survive on tobacco. Adult production on cotton polyhedral virus against both H. zea a n d Heliothis was about four times as great as on maize. How• virescens (F.) and found that the control provided ever, Sparks et al. (1971) reported that corn, partic• was comparable to that obtained with methyl para- ularly a multi-eared sweet corn, produced about thion, alone or in combination with ethyl parathion. five times as many corn earworms as cotton. The advantage that farmers gain in using cultural Some of the basic insect-plant interactions control with susceptible varieties would certainly within the crop occur at the plant level. Although be enhanced when combined with the resistant many interactions may occur between crops, little varieties. The use of early-planted resistant corn research has been initiated in this area on a field hybrids has been recommended for many years in basis to demonstrate those insect-crop interac- the southern United States as a complementary tions.The insect and within-crop interactions will be practice with the resistance to evade damaging discussed on the basis of the three mechanisms of corn earworm populations. Adkisson and Dyck resistance (Fig. 5). (1980) stated that resistant varieties, including those that can be manipulated to evade pest attack, are highly desirable in a cultural control system designed to maintain pest numbers below the economic threshold while preserving the natu• ral enemies. They presented a model to illustrate the impact of a resistant nectariless cotton on a pink bollworm, Pectinophora gossypiella (Saund• ers), population, and then combined this with the early short-season resistant nectariless variety to demonstrate the additional advantages of combin• ing control components such as resistant varieties and cultural control.

Crop-Insect Interactions

Crop-insect interactions may occur at several dif• ferent levels, i.e., between or among different crop species or between different varieties within a crop species, within a field planted to a resistant variety, and finally at the plant level. Johnson et al. (1975) reported that many qualita• tive observations have been made on the interac• Nonpreference tion of host plants with adult H. zea. Host factors included the fitness of the host, variety of the host, Figure 5. Plant x pest interactions occurring number and acreage of the host crops, and the with nonpreference and/or antibiosis mecha• phenological status of the host. Ovipositional nisms of resistance.

2 1 5 Tolerance research on the influence of plant pubescence on Heliothis-crop interactions. Lukefahr et al. (1971) A crop or plant may be tolerant if it is able to yield showed oviposition suppression of more than 60% well despite infestations that seriously damage on Heliothis spp from the use of nonpreferred gla• susceptible plants (Painter 1968). Interactions brous cotton strains. Any eggs laid were also easily between the pest and the resistant variety are not dislodged; this, plus the nonpreference, was asso• considered to occur, since this phenomenon is ciated with the overall resistance effect. Robinson entirely a plant response. However, the use of the et al. (1980) reported that significantly fewer H. tolerant variety offers the grower several alterna• virescens eggs were laid on smooth-leaf cotton tive methods of pest control: (1) pesticides at than on pubescent cotton, whether or not the reduced rates (McMillian et al. 1972; Wiseman et al. tobacco budworm had a choice of hosts. Cosenza 1973); (2) parasites or predators (Starks et al. 1972, and Green (1979) found that the resistance of the 1974); (3) cultural control; and (4) insect pathoge n s fruit of a breeding line of tomato (entry 38) was (Fernandez et al. 1969). Therefore, a number of nonpreference by a 10:1 ratio over Chico III. Leuck interactions may occur when control components et al. (1977) reported that H. zea laid significantly are added to the resistant variety in controlling the fewer eggs (11.8 vs 88.2%) on foliage of a tri- pest, especially depending upon whether the var• chomeless near-isogenic Tift 23S (tr tr) pearl millet, iety has low, intermediate, or high tolerance to the Pennisetum americanum (L.) Leake, than on insect. pubescent foliage of Tift 23H (Tr Tr) (Fig. 7). Panda and Daugherty (1975) demonstrated that H. armigera showed nonpreference of dense pubescent Nonpreference soybean leaves by a ratio of more than 3:1 after 24 h exposure. Wiseman et al. (1976b) first found that Antigua 2D-118 possessed leaf-feeding resist• A crop or variety may be nonpreferred when it a n c e to H. zea. Then Widstrom et al. (1979) showed possesses plant characters that stimulate insect (Fig. 8) that Antigua 2D-118 had fewer trichomes responses resulting in a particular plant or variety than Cacahuacintle, a susceptible entry. They also being used less than another for oviposition, for found (Table 2) that about 25% fewer eggs were food, for shelter, or for combinations of the three deposited on Antigua 2D-118 leaves. (Painter 1951). A number of reports exist that deal with nonpref• Wiseman et al. (1978b) studied some of the corn e r e n c e a n d Heliothis interactions (Fig. 6). Webster earworm larvae behavioral movements on sus• (1975) cited a number of papers that reported ceptible and resistant corn. They found that due to

P e s t

Ovipositional behavior F e e d i n g behavior Resistant stimuli

p h y s i c a l c h e m i c a l Orientation Orientation g l a b r o u s m a y s i n t a c t i l e gossypol nectariless t a n n i n s f l a v o n o i d s Recognition I n c i t a n t

Oviposition Continual feeding

Nonpreference-Antibiosis

Figure 6. Illustrations of some of the Interactions that occur with nonpreference and antibiosis as mechanisms of resistance.

2 1 6 Figure 7. Heliothis zea oviposition on pearl millet; A: 23S (trtr);B:23S(TrTr). (Source: Leuck et al. 1977.)

a lack of significant thigmotactic stimuli by the sus• evaluated, reductions of up to 80% in eggs of Helio• ceptible corn, larvae penetrated the corn silks this spp were found in 1969 (Lukefahr et al. 1971). deeper before initial feeding began. Conversely, on the resistant silks, larvae penetrated only slightly Antibiosis into the silk channel before feeding was initiated (Table 3). On the two resistant corns, one tolerant A plant or variety may be antibiotic if it either pos • and the other antibiotic, initial movement was sim• sesses a material injurious to the pest that feeds on ilar. However, the tolerant corns possessed a tight it or if the plant part fed on lacks some necessary silk channel with a large amount of silk that main• nutrient (Painter 1968). Antibiosis in plants may be tained high moisture over the period of larval devel• evaluated by several insect responses: (1) death of opment. These factors, combined with the absence early instars; (2) decreased larval weights; (3) pro• of antibiotic chemicals, contributed to the fact that longed life; (4) failure to pupate; and (5) less the silks were consumed by corn earworms, result• fecundity. ing in little, if any, ear damage (Wiseman et al. A number of examples have been cited of antibi• 1977). osis influencing insect-plant interactions. Panda Other cotton plant morphological characters and Daugherty (1975) reported that resistant soy• affect Heliothis spp oviposition and eventually are beans had an antibiotic effect on corn earworm less damaged (Maxwell et al. 1972). In field studies, development. When lyophilized green pod material Lukefahr et al. (1965) found that the absence of of susceptible and resistant (antibiosis type) soy• extrafloral nectaries on the cotton plant (nectari- beans was used in a diet for corn earworm, devel• less) caused as much as a 64% reduction in egg opmental time of larvae fed on the resistant type laying by Heliothis spp moths. When both glabrous was more than twice as long as that of larvae fed on and nectariless characters were combined and the susceptible type.

2 1 7 Figure 8. H. z e a egg placement in relation to leaf trichomes. (Source: Widstrom et al. 1979.)

Quercetin inhibited the growth of H. zea larvae, and Table 2. Ovipositlonal placement and numbers of killed more than 70% of H. virescens larvae. a com earworm eggs per leaf on leaves of two exotic Kennedy and Yamamoto (1979) using chloro• com selections. form as a solvent, extracted from the foliage of a wild tomato, Lycopersicon hirsutum F. glabratum, S e l e c t i o n PI-134417, a concentrate that was toxic to H. zea

Leaf region A n t C a c . C Mean larvae; 2 hours exposure to the extract killed 100% of the larvae. Williams et al. (1980) identified the extract as 2-tridecanone and labeled it as a natu• T i p 0 . 7 7 a 1.00 a 0 . 8 8 a rally occurring insecticide. It appears that the 2- M i d d l e 1.75 b 2 . 3 5 b 2 . 0 5 b tridecanone is the chemical basis of the antibiosis Base 0.62 a 0.91 a 0 . 7 7 a found in this wild tomato. Campbell and Duffy (1979) found that a -tomatine, a resistance chemi• Source : Widstrom et al. (1979). cal found in tomatoes, was toxic to both H, zea a n d a. Means within any column followed by to an endoparasite, Hyposoter exiguae (Viereck), different letters are significantly different of H. zea. Thus, the potential incompatibility of plant at the 1% level of probability. resistance and certain biological controls exists. However, this appears to be only an isolated case of incompatibility. Lukefahr and Martin (1966) and Shaver and Recent research on H. zea and corn has shown Lukefahr (1969) showed the effects of cotton pig• that antibiosis resistance is present in the silks of ments (gossypol and flavonoid pigments) on the Zapalote Chico #2451 (Wiseman et al. 1976a, development of Heliothis spp. Less than 30% of the 1977), and that the resistance is high enough to larvae of H. zea and H. virescens reached the pupal reduce corn earworm numbers by four-fold (Wise- stage when the diet contained 0.2% gossypol. man et al. 1978a). Waiss et al. (1979) discovered a

218 Table 3. Average locationa of corn earworm larvae on both resistant (R) and sus ceptible (S) corns after 3, 6, 9, and 12 days Infestation in 1975, Tifton, Ga, USA.

Days after infestationb

Corn cultivar 3 6 9 1 2

Zapalote Chico # 2451 (R) 0 . 8 3 a 0 . 8 3 a 0 . 9 9 a 1 . 2 9 a 471-U6 X 81-1 (R) 1 . 0 3 a 1 . 2 1 a 1 . 6 7 a b 2 . 5 9 b Dixie 18 (R) 0 . 9 3 a 1 . 1 7 a 1 . 7 3 b 2 . 1 3 b Asgrow A204 (S) 1 . 2 4 a 2 . 4 3 b 3 . 2 7 c 4 . 1 3 c Stowell's Evergreen (S) 1 . 0 3 a 3 . 3 2 c 5 . 2 4 d 5 . 0 7 d l o a n a (S) 2 . 5 5 b 5 . 0 3 d 6 . 0 9 e 7 . 0 5 e

Source: Wiseman et al. (1978) a . Location of earworm larvae was based on 0 = no infes tation, 1 = larvae in upper 1/3 of silk channel, 2 = larvae in the mid 1/3 of silk channel, 3 = larvae in lower 1/3 of silk channel. 4 = larvae on ear tip feeding on silk, 5 = larvae o n ear tip feeding on ear, and 6-n = larval penetration down ear at increments of 1 cm. b . Means of earworm location within any sample date foll owed by the same letter are not significantly different at P = 0.05. Means include a n average of 10 ears/replication for three separate plantings in 1975.

flavone glycoside, called maysin, in the silks of Z. ant to insects and certainly could have an impor• Chico that retards corn earworm larval growth. tant effect on management of insect populations. When the larvae enter the silks of Z. Chico, they Jermy et al. (1968) demonstrated that host begin to feed near the ear tip; some of the larvae induction could affect host preference by H. zea "girdle" the silks, causing the outer silks to drop larvae. They found that the induced preference from the ear, leaving the larvae exposed to the was specific for the inducing plant and that it was environment. Generally, the silks have deteriorated not eliminated by larval molts or subsequent feed• in quality by this time and the larvae probably cra w l ing. The implications here are numerous, but in the out of the ears and die. This condition may be a c a s e of Heliothis, the crop on which larvae have result of a combination of antibiosis and nonprefer- developed is not available for the next generation ence. Laboratory data (unpublished) showed that (e.g., corn or early-season hosts). Therefore, pref• larvae placed on silks of Z. Chico and in the near erence induction would have limited implications vicinity of susceptible silks will migrate to the mo r e for many situations involving Heliothis. However, acceptable silks. Thus, nonpreference could very the multihost Heliothis could be drastically affected well be a factor in the overall resistance of Z. Chico. biologically (antibiosis) on one crop and then com• pletely recover during the next generation from the previous effects because it developed on a com• Plant Nutrition and Plant Induction pletely different host. Heliothis management then will necessitate plant resistance to be developed in several crop species. On the other hand, Takata A number of researchers have reported the influ• (1961) reported that in the cabbage butterfly, Pieris ence of plant nutrition on insect oviposition and rapae crucivora (Boisduval), rearing for succes• feeding responses. Leuck et al. (1974) stated that sive generations on the same host influenced the micronutrients or trace elements in soils may pro• ovipositional preference of the adults. Adults that duce some important ecological and biological were reared on cabbage for several successive effects induced in crop plants and insect generations tended more and more to avoid cab• populations—effects that are often attributed to bage for oviposition. If this situation could be sh o w n such expressions of host-plant resistance as non- for Heliothis, then the development of monocul• preference, antibiosis, or tolerance. Indeed plant tures in certain areas might prove beneficial in nutrients may influence the search for plants resist•

2 1 9 Heliothis ovipositional preference and eventual GOSENZA, G.W., and GREEN, H.B. 1979. Behavior of population reduction. the tomato fruitworm, Heliothis zea (Boddie) on suscepti• ble and resistant lines of processing tomatoes. Hor t - science 14:171-173. Conclusions DAHMS, R.G. 1972a. The role of host plant resistance in

Several aspects and uses of an insect-resistant integrated insect control. Pages 152-167 in The control of the shoot fly, eds. M.G. Jotwani and W.R. Young. Ne w variety have been discussed along with the impli• Delhi, India: Oxford and IBH. cations of interactions that could occur, especially when nonpreference and antibiosis mechanisms DAHMS, R.G. 1972b. Development of crop resistance of resistance are present in the crop variety. to insects. Journal of Environmental Quality V. 28- 3 4 . Dahms (1972a) gave several theoretical examples FERNANDEZ, AT., GRAHAM, H.M., LUKEFAHR, of effects of resistant plants on a developing aphid M.J., BULLOCK, H.R., and HERNANDEZ, N.S., Jr. population. With an initial infestation of one to two 1 9 6 9 . A field test comparing resistant varieties plus ap p l i • aphids per plant, and assuming no nymphal mortal• cations of polyhedral virus with insecticides for c o n t r o l of ity, an adult reproduction rate of one per day for 20 Heliothis spp. and other pests. Journal of Economic Ento• days, and nymphal maturation in 10 days, twice as mology 62:173-177. many aphids would survive on a susceptible cul- GROSS, H.R., Jr., WISEMAN, B.R., and McMILLIAN, tivar in comparison to a nonpreferred one after 50 W . W . 1 9 7 6 . Comparative suitability of sweet corn for d a y s . T h e n a s o n e e x a m p l e o f m a n y o n antibiosis, establishment by larvae of the corn earworm. Enviro n • he s h o w e d the effect of n y m p h a l mortality at the mental Entomology 5: 955-958. end of 50 days. Assuming 10% mortality, the antibi• HOLCOMB, R.W. 1970. Insect control: alternatives to osis w o u l d result in ca. 3 0 % fewer insects, a 5 0 % the use of conventional pesticides. Science 168: 45 6 - mortality would result in over 90% fewer insects, 4 6 0 . but it w o u l d require in e x c e s s of 9 0 % mortality to HORBER, E. 1972. Plant resistance to insects. USDA prevent an insect increase. Agricultural Science Review 10: 1-18. Single-factor approaches in the management of IGNOFFO, C.M., HOSTETTER, D.L., BIEVER, K.D., Heliothis spp are apparently inadequate. However, GARCIA, C., THOMAS, G.D., DICKERSTON, W.A., the wise use of the resistance factors or mecha• and PINNELL, R. 1978. Evaluation of an entomopatho- nisms within each crop, coupled with the timely genic bacterium, fungus, and virus for control of Heliothis manipulations of other compatible components of zea on soybeans. Journal of Economic Entomology 71 : integrated pest management should suppress 1 6 5 - 1 6 8 . insect density levels below those causing eco• JERMY, T., HANSON, F.E., and DETHIER, V.G. n o m i c injury. T h e d e v e l o p m e n t a n d use of resistant 1 9 6 8 . Induction of specific food preferences in lepidop- cultivars will play an important role in the future terous larvae. Entomologia Experimental et Applicat a d e v e l o p m e n t of plant protection against Heliothis 11:211 -230. spp, and especially in the implementation of inte• grated pest management systems. JOHNSON, M.W., STINNER, R.E., and RABB, R.L. 1975. Ovipositional response of Heliothis zea (Boddie) to its major hosts in North Carolina. Environmental En t o m o l - References ogy 4: 291 -297. KENNEDY, G.G., and YAMAMOTO, R.T. 1979. A toxic ADKISSON, P.L., and DYCK, V.A. 1980. Resistant var- factor causing resistance in a wild tomato to the t o b a c c o ieties in pest management systems. Pages 233-251 in hornworm and some other insects. Entomologia Experi • Breeding plants resistant to insects, eds. F.G. Max w e l l mentalis et Applicata 26: 121-126. and PR. Jennings, New York, USA: Wiley. 683 pp. KOGAN, J., SELL, D.K., STINNER, RE., BRADLEY, CAMPBELL, B.C., and DUFFEY, S.S. 1979. T o m a t i n e J.R. Jr., and KOGAN, M. 1978. The literature of arthrop• and parasitic wasps: Potential incompatibility of plant ods associated with soybeans. V. A bibliography of H e l i o - antibiosis with biological control. Science 205: 70 0 - 7 0 2 . this zea (Boddie) and H. virescens (F.) (Lepidoptera: Noctuidae). International Agriculture Publications CATE, J.R., BOTTRELL, D.G., and TEETES, G.L. INTSOY Series 17, University of Illinois, Urbana, III, USA. 1 9 7 3 . Management of the greenbug on grain sorghums. 2 4 2 pp. 1. Testing foliar treatments of insecticides agains t g r e e n - bug and corn leaf aphid. Journal of Economic Entomo l o g y LEUCK, D.B., WISEMAN, B.R., and McMILLIAN, 66:945-951. W . W . 1 9 7 4 . Nutritional plant sprays: effect on fall army-

2 2 0 worm feeding preferences. Journal of Economic Ento• PANDA, N., and DAUGHERTY, D.M. 1975. Note on the mology 67: 58-60. antibiosis factor of resistance to corn earworm in pubes• cent genotypes of soybean. Indian Journal of Agricultural LEUCK, D.B., BURTON, G.W., and WIDSTROM, N.W. Sciences 45: 68-72. 1977. Insect oviposition and foliage feeding resistance in pearl millet. Journal of the Georgia Entomological Society PRETORIUS, L.M. 1976. Laboratory studies on the 12: 138-140. development and reproductive performance of Heliothis armigera (Hubn.) on various food plants. Journal of the LUGINBILL, P., Jr. 1969. Developing resistant plants— the ideal method of controlling insects. U.S. Department Entomological Society of South Africa 39: 337-343. of Agriculture production research report 111, Washing• REFAI, A. EL. EL-GUINDY, M.A., and ABDEL- ton, DC, USA. 14 pp. SATTAR, M.M. 1979. Variation in sensitivity to insecti• cides of Heliothis armigera Hbn. fed on different host LUGINBILL, P., Jr., and KNIPLING, E.F. 1969. Sup• plants Zeitschrift fur 'Angewandte Entomologie 88: 107- pression of wheat stem sawfly with resistant wheat. U.S. 111. Department of Agriculture production research report 107, Washington DC, USA. 9 pp. ROBINSON, S.H., WOLFENBARGER, D.A., and DIL- DAY, R.H. 1980. Antixenosis of smooth leaf cotton to the LUKEFAHR, M.J., HOUGHTALING, J.E., and GRA• ovipositional response of tobacco budworm. Crop HAM, H.M. 1971. Suppression of Heliothis populations Science 20: 646-649. with glabrous cotton strains. Journal of Economic Ento• mology 64: 486-488. SCHALK, J.M., and RATCLIFFE, R.H. 1976. Evalua• tion of ARS program on alternative methods of insect LUKEFAHR, M.J., and MARTIN, D.F. 1966. Cotton- control: host plant resistance to insects. Bulletin of the plant pigments as a source of resistance to the bollworm Entomological Society of America 22: 7-10 and tobacco budworm. Journal of Economic Entomology 59: 176-179. SHAVER, T.N., and LUKEFAHR, M.J. 1969. Effect of flavonoid pigments and gossypol on growth and develop• LUKEFAHR, M.J., MARTIN, D.F., and MEYER, J.R. ment of the bollworm, tobacco budworm and pink boll- 1965. Plant resistance to five Lepidoptera attacking cot• worm. Journal of Economic Entomology 62; 643-646. ton Journal of Economic Entomology 58: 516-518. SPARKS, A.N., WISEMAN, B.R., and McMILLIAN, MAXWELL, F.G. 1972. Host plant resistance to W.W. 1971. Production of corn earworms on several insects—nutritional and pest management relationships. hosts in field cages. Journal of Economic Entomology 64: Pages 599-609 in Insect and mite nutrition. Amsterdam: 540-541. North Holland. STARKS, K.J., MUNIAPPAN, R., and EIKENBARY, MAXWELL, F.G., JENKINS, J.N., and PARROTT, W.L. R,D. 1972. Interaction between plant resistance and par• 1972. Resistance of plants to insects. Advances in asitism against the greenbug on barley and sorghum. Agronomy 24: 187-265. Annals, Entomological Society of America 65: 650-655. McMILLIAN, W.W., WISEMAN, B.R., WIDSTROM, STARKS, K.J., WOOD, E.A. Jr., and BURTON, R.L. N.W., and HARRELL, E.A. 1972. Resistant sweet corn 1974. Relationships of plant resistance and Lysiphlebus hybrid plus insecticide to reduce losses from corn ear- testaceipes to population levels of the greenbug on grain worms. Journal of Economic Entomology 65: 229-231. sorghum. Environmental Entomology 3: 950-952. MOHAMED, A.K.A., BELL, J.V., and SIKOROWSKI, TAKATA, N. 1961. Studies on the host preference of the P.P. 1978. Field cage tests with Nomuraea rileyi against common cabbage butterfly, Pieris rapae crucivora (Bois- corn earworm larvae on sweet corn. Journal of Economic duval). XII. Successive rearing of the cabbage butterfly Entomology 71: 102-104. larva with certain host plants and its effect on the oviposi• PAINTER, R.H. 1951. Insect resistance in crop plants. tion preference of the adult. Japan Journal of Ecology 11: New York, USA: Macmillan. 520. pp. 147-154.

PAINTER, R.H. 1966. Plant resistance as a means of TEETES, G.L. 1976. Integrated control of arthropod controlling insects and reducing their damage. Pages pests of sorghum. Pages 24-41 in Proceedings, US-USSR 138-148 in Pest control by chemical, biological, genetic, Symposium: The integrated control of arthropod, disease and physical means—A symposium. USDA-ARS-33-110, and weed pests of cotton, grain sorghum and deciduous U.S. Department of Agriculture, Washington, DC, USA. fruit. Texas Agricultural Experiment Station miscellane• 214 pp. ous publication 1276, College Station, Tex, USA. 216 pp.

PAINTER, R.H. 1968. Crops that resist insects provide a TEETES, G.L. 1980. Breeding sorghum resistant to way to increase world food supply. Kansas Agricultural insects. Pages 457-485 in Breeding plants resistant to Experiment Station Bulletin 520, Manhattan, Kans, USA. insects, eds. F.G. Maxwell and P.R. Jenning. New York, 22 pp. USA; Wiley. 683 pp.

221 THOMAS, R.O., CLEVELAND, T.C., and CATHEY, WISEMAN, B.R., WIDSTROM, N.W., and McMILLIAN, G . W . 1 9 7 9 . Chemical plant growth suppressants for N.W. 1978b. Movement of corn larvae on ears of resist• reducing late-season cotton bollworm-budworm feeding ant and susceptible corns. Environmental Entomology sites. Crop Science 19:861-863. 7 : 7 7 7 - 7 7 9 .

WAISS, A.C., Jr., CHAN, B.G., ELLIGER, C.A., WISE- MAN, B.R., McMILLIAN, W.W., WIDSTROM, N.W., ZUBER, M.S., and KEASTER, A.J. 1979. M a y s i n , a fla- v o n e g l y c o s i d e f r o m c o r n silks w i t h a n t i b i o t ic activity toward corn earworm. Journal of Economic Entomology 72:256-258.

WEBSTER, J.A. 1975. Association of plant hairs and insect resistance—an annotated bibliography. U.S. Department of Agriculture miscellaneous publication 1297, Washington DC, USA. 18 pp.

WIDSTROM, N.W., McMILLIAN, W.W., and WISE- MAN, B.R. 1979. Ovipositional preference of the corn e a r w o r m a n d t h e d e v e l o p m e n t o f t r i c h o m e s o n t w o e x o t i c corn selections. Environmental Entomology 8:833-839.

WILLIAMS, W.G., KENNEDY, G.G., YAMAMOTO, R.T., THACKER, J.D., and BORDNER, J. 1980. 2 - tridecanone: A naturally occurring insecticide from the w i l d t o m a t o Lycopersicon hirsutum F. glabratum. S c i e n c e 207:888-889.

WISEMAN, B.R., and MORRISON, W.P. 1981. C o m • ponents for management of field corn and grain sorghum i n s e c t s a n d m i t e s i n t h e U n i t e d States. U S D A - A R S S R Publication A106.12: ISSN0193-3779, U.S. Department of Agriculture, Washington, DC, USA.

WISEMAN, B.R., McMILLIAN, W.W., and WID• STROM, N.W. 1972. Tolerance as a mechanism of res• i s t a n c e i n c o r n t o t h e c o m e a r w o r m . J o u r n a l o f E c o n o m i c Entomology 65:835-837.

WISEMAN, B.R., HARRELL, E.A., and McMILLIAN, W . W . 1 9 7 3 . Continuation of tests of resistant sweet corn h y b r i d p l u s i n s e c t i c i d e s t o r e d u c e l o s s e s f r o m c o r n e a r - worm. Environmental Entomology 2:919-920.

WISEMAN, B.R., McMILLIAN, W.W., and WID• STROM, N.W. 1976a. F e e d i n g o f c o r n e a r w o r m i n t h e laboratory on excised silks of selected corn entries, w i t h n o t e s o n O n u s insidiosus. Florida Entomologist 59-305- 3 0 8 .

WISEMAN, B.R., WIDSTROM, N.W., McMILLIAN, W.W., and PERKINS, W.D. 1976b. G r e e n h o u s e e v a l u a • t i o n s o f l e a f - f e e d i n g r e s i s t a n c e i n c o r n t o t h e c o r n e a r - worm. Journal of the Georgia Entomological Society 1 1 : 6 3 - 6 7 .

WISEMAN, B.R., WIDSTROM, N.W., and McMILLIAN, W . W . 1 9 7 7 . Ear characteristics and mechanisms of res• i s t a n c e a m o n g s e l e c t e d c o r n s t o t h e c o r n e a r w o r m . Flor• ida Entomologist 60:97-103.

WISEMAN, B.R., McMILLIAN, W.W., and WID• STROM, N.W. 1978a. Potential of resistant com to reduce corn earworm production. Florida Entomologist 6 1 : 9 2 .

2 2 2 A Review of the Problems, Progress, and Prospects for Host-Plant Resistance to Heliothis Species

M.J. Lukefahr*

Abstract

The development of insecticidal resistance in the 1960s led to increased support tor host- plant resistance (HPR) projects. As a result, sources of plant resistance in all the major crops were identified. However, identification of resistance factors was based on laboratory studies, and work never progressed to where field suppression of Heliothis populations was demonstrated. A brief review, with references to the major works and their impact on the field of host-plant resistance, is presented. The prospects for use of host-plant resistance in crops with high production inputs and high fixed costs are not good. The synthetic pyrethroids are highly effective and result in stable yields; their use requires very little manage• ment, and in such crops, these chemicals will probably dominate the pest-control strategies. Crops of low cash value or those grown in regions where pesticides are not part of the pro• duction system are the ones in which the use of host-plant resistance is thought to have a potential impact.

T h e g e n u s Heliothis probably contains the most host-plant resistance was first applied against Heli• important insect complex in the world trom the othis zea in corn, since this was the major crop standpoint of crop loss. The noctuid pest species of affected by Heliothis spp in the United States. This this complex exhibit wide host ranges, high fecun• work identified several plant characteristics that dity, and ability to move long distances, thereby resulted in partial resistance. However, the efficacy spanning several crops and seasons. One or more and convenience of insecticides resulted in a de- species can cause economic losses to soybeans, emphasis of host-plant resistance studies. When cotton, t o b a c c o , c o r n , tomato, s o r g h u m , groundnut, control of H. virescens became extremely difficult and many other plants, both wild and cultivated, on with recommended insecticides in the early 1960s, which they are able to reproduce. interest in host-plant resistance was renewed, as it As stated by Kogan et al. (1978) the principle of appeared that this may be the only means by which populations could be reduced to subeconomic levels.

*International Institute of Tropical Agriculture, Ibadan, Nigeria. The resistance to pesticides in Heliothis spp cor-

International Crops Research Institute tor the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. 2 2 3 responded with the awareness of environmental Vegetables problems associated with high pesticide use, resulting in support for host-plant resistance pro• In an excellent review of insect resistance in veget• jects. Reported in this paper are the results able and fruit crops (Kennedy 1978), tomato was achieved against Heliothis in some of the major the only crop mentioned as having any known res• crops attacked by Heliothis spp. istance to Heliothis. Both H. zea a n d H. virescens attack tomato and are called tomato fruitworms. The females deposit Soybeans the eggs on foliage, and the early instars feed on foliage before attacking the fruit. Fery and Cuthbert Soybeans are grown in several countries; however, (1973,1974) found that plant density, vine size, and the USA and Brazil are the major commercial pro• earliness are all associated with percentage of d u c e r s of this crop. damaged fruit. When the variability due to these Heliothis zea a n d H. virescens are pests of s o y • factors was considered, no differences were found beans, and are commonly referred to as pod- when 1030 lines were evaluated. However, the worms; however, larvae are able to complete same authors (1975) reported high levels of antibi• d e v e l o p m e n t in plants that have not set pods. In osis in the wild Lycopersicon hirsutum, f. glabra- these cases, the foliar damage does not appear to tum. Intact plants and excised foliage gave similar result in yield losses, as plants can easily compen• results. This species was reported to be compatible sate for the damage at this stage. with cultivated tomatoes, so presumably this source of resistance could be utilized in a host- Cultural practices such as narrow-row planting plant resistance breeding program. (75 cm) result in a closed canopy when pods are f o r m e d, a n d Heliothis have never been recorded as Lange and Bronson (1981) in their review of damaging pods after the canopy has closed (J.R. insect pests on tomato list an economic threshold Bradley personal communication). of 0.25 to 0.50% damaged green fruit for commer• However, when plant growth is reduced, due to cial tomato production. If a commercial crop can late planting or drought, Heliothis c a n c a u s e tolerate so little damage, it seems unlikely that a losses. The early instars feed on foliage, the later resistant tomato cultivar can be developed, as ones (third instar onwards) on pods. near-immunity to insect attack would be required. The economic threshold for Heliothis in soybean has been established at 6.5 larvae per meter of row (Mueller and Engroff 1980). Cotton Clark et al. (1972) f o u n d that t w o plant introduc• tions into the USA reduced populations of H. zea on It has been' estimated that nearly 30% of all pesti• soybean. PI-171451 showed reduced oviposition, cides manufactured in the world are used to control presumably due to nonpreference; PI-227687 Heliothis spp on cotton. So successful were chemi• showed the lowest percentage of pod damage- cal pesticides in increasing and stabilizing yields, even though oviposition was heavy—probably that for approximately 15 years no other method of because of antibiosis. controlling cotton insects was given serious con• Beland and Hatchett (1976) reported on feeding sideration. By 1965, high levels of resistance to trials of H. zea developing on leaves of PI-229358, both the chlorinated hydrocarbons and carbamate which gave significant reductions in larval growth insecticides were found (Lowry 1966), and by 1970 over the control, cv Davis. H. virescens field populations were exhibiting two- Dreyer et al. (1979) isolated pinitol from the to five-fold levels of resistance to methyl parathion leaves of both PI-229358 and cv Davis, and the (Wolfenbarger et al. 1971). Parallel situations had authors believed this compound may be involved in also occurred in Australia and Central and South resistance to H. zea as well as the Mexican bean A m e r i c a . However, e v e n before 1965, it b e c a m e beetle (Epilachna varivestis Mul.). However, other obvious that alternative methods of population sup• compounds are probably also involved, as the dif• pression were necessary, and research into host- ference between the susceptible standard and res• plant resistance received support. istant line was very small and concentrations An evaluation of several plant characters in cot• required to reduce growth by 50% seem unusually ton showed three that resulted in measurable lev• large. els of population suppression.

2 2 4 Morphological Characters dators, which then removes some of the con• straints on Heliothis population (Schuster et al. 1976). Nectariless

Cotton cultivars have conspicuous nectary glands Glabrous on the veins and beneath the flowers and bolls; these nectaries secrete copious amounts of sugar, Most commercial varieties of cotton grown in the which furnish food for Heliothis adults. It has been USA have approximately 2000 trichomes per demonstrated that if adults are unable to obtain square inch (about 310/cm2 ) on the terminal food, their longevity and fecundity are reduced by leaves, which is the preferred oviposition site of approximately 50% (Lukefahr and Martin 1964). A Heliothis spp on cotton. If the trichome number is wild cotton from Hawaii lacks this extrafloral nec• reduced to 200/square inch (30/cm2 ), at least a tary system and this character was transferred into 50% reduction in egg and larval populations (Table Gossypium hirsutum by Meyer and Meyer (1961). 1) can be achieved (Lukefahr et al. 1966, 1971, Numerous cage and field tests have been con• 1975). While the value of this character for Heliothis ducted to evaluate this character. In cage tests, suppression has been demonstrated, it is known to where the movement of Heliothis can be regulated, increase susceptibility to plant bugs (Schuster et al. the number of eggs and larvae is reduced by 1976) and leaf-hoppers (Parnell et al. 1949). How- approximately 50%. However, in field plots of about ever, not all glabrous lines show the same degree 2 ha, there is no measurable reduction in Heliothis of susceptibility to these pests, and further populations. These differences are probably due to research is needed to evaluate additional glabrous the flight habits of Heliothis adults, as feeding can sources. take place at sites widely separated from ovipositional sites. If nectariless cotton was grown over large areas (over 40 ha), reduction may be Early e x p e c t e d . Indirectly, the nectariless character does result The concept of earliness as a means of escaping in Heliothis suppression, as it effectively lowers Heliothis injury was first discussed by Pearson plant bug populations. The chemical control of (1958). The value of this characteristic has been these early-season bugs eliminates Heliothis pre- demonstrated by Walker and Niles (1971) and by

Table 1. Suppression of Heliothis spp in field tests with glabrous cotton.

Heliothis/ha

Year Cotton type No. of eggs No. of larvae

1 9 6 5 C o m m e r c i a l 43 037 56 078 G l a b r o u s 23 776 3 0 4 3 0

1 9 6 6 C o m m e r c i a l 102 5 3 9 G l a b r o u s 77 108

1967 C o m m e r c i a l 31 951 5 4 9 7 G l a b r o u s 12 0 8 0 3 4 7 7

1 9 6 8 C o m m e r c i a l 41 4 2 5 42 9 0 5 G l a b r o u s 16 106 22 953

1 9 6 9 C o m m e r c i a l 74 4 8 7 6 9 137 G l a b r o u s 11 772 2 0 8 6 9

Reduction (%) 52 58

2 2 5 Heilman et al. (1977). These early-fruiting types have the ability to set a crop in a shorter period of Table 2. ED 50 values of heliothis against Heliothis virescens larvae. time than conventional varieties and can also com• pensate for fruiting forms that are lost due to insect injury. The most successful program in developing C o m p o u n d M g / g d i e t these varieties is Texas A & M University's TAM- COT Cotton Program (Bird et al. 1968). Basically, G o s s y p o l 0.8 these cottons mature sufficiently early to escape Hemigossypolone 1 0 . 5 the last, and often most damaging, generation of Heliocide H1 2 . 5 Heliothis attack. The yield is comparable to full- H 2 1 1 . 2 season cultivars. H3 3 . 9

H 4 U n s t a b l e

Plant Chemistry

ant lines had different combinations and concen• Gossypol trations of the various terpenoids. The assumed advantage to the plant in possessing such an All cotton species contain a terpenoid aldehyde, assortment of chemicals would be to marshal a gossypol, a compound known to be toxic to warm- number of toxic agents against one or more insect blooded animals. A major effort was made to pests that feed on it. (Table 2 summarizes the ED remove gossypol genetically from cotton; however, 50 values of these compounds). the gossypol-free cottons that were successfully developed turned out to be very susceptible to Heliothis attack. Condensed Tannins Most cotton cultivars have a gossypol content of about 0.5% (dry weight) and this level causes no Two primitive G. hirsutum race stocks, designated appreciable mortality or growth reduction. How• as Texas 194 and Texas 254, consistently pro• ever, when this level is increased to 1.2% or above, d u c e d H. virescens larvae that were approximately at least a 50% larval mortality results (Lukefahr et one-half the size of the standard. The antibiotic al. 1966). When gossypol is added to larval diets, a factor was unrelated to gossypol or the heliocides. much lower concentration is required to achieve Chan et al. (1978) identified the active component this same level of mortality. However, on the plant, of Texas 254 as a condensed tannin. A concentra• the larvae are able to feed selectively on parts that tion of 0.2% in larval diet of H. virescens s u p • have the lowest gossypol content, such as the pressed larval growth by 84% (Table 3). Schuster pollen, anthers, and stigma. (1980) identified the Heliothis-resistant factor in several lines of cotton as condensed tannins. How• ever, what is not clear is that many of these lines also possessed high levels of terpenoids. Heliocides

Beginning in 1976, an effort was made to grow the entire race stock collection of Gossypium hirsutum and bioassay plant parts for Heliothis resistance. Table 3. Effect of condensed tannin on H. virescen This was essentially achieved, and about 3% of the larvae. lines were found to give growth inhibition and/or Mean larval weight larval mortality when compared with standard cul- Tannin in diet (mg) after 7 days tivars. Based on gossypol analyses, it was appar- T e s t 1 T e s t 2 ent that gossypol was the biologically active agent, (%) but in at least nine lines, other chemical factors were involved. Eventually, five compounds, desig- 0 . 0 0 2 9 9 2 6 6 nated as heliocides, were identified and bioas- 0.1 2 6 0 2 0 7 84 45 sayed for biological activity against Heliothis (Gray 0.2 37 2 0 et al. 1976; Stipanovic et al. 1977). The nine resist - 0.3

2 2 6 Maize tially the same conclusion has been reported by Guthrie and Walter (1961), Zuber et al. (1971), The literature appears to be filled with anomalies Starks and McMillian (1967), and Wiseman et al. regarding economic threshold levels as well as (1970). On the contrary, Del Valle and Miller(1963) sources of resistance in maize. found that husk length and tightness were not res- In South America, particularly Peru, numerous istance mechanisms, but only a chance occur- references show that H. virescens is a pest of rence when related to Heliothis resistance. maize, while in other countries of its range, it Luckman et al. (1964) found that silk balling was appears to be an "accidental" pest, as only a small associated with H. zea resistance, as it formed a percentage of the entire Heliothis collection have physical barrier to larval penetration. Zuber et al. been identified as H. virescens. In Africa, Europe, (1971) concluded that the longer and tighter silk Australia, and Asia, H, armigera is the recorded channels were probably a mechanism of resist• pest on maize. ance, as more larvae completed development in It would appear that in field corn, Heliothis results silk channels before reaching the kernels. Knapp et in very small yield losses, as feeding is restricted to al. (1965) found a lower concentration of amino the tip of the ear, and damage probably does not acids and reducing sugars in silks of resistant exceed 2% of the kernels (Starks et al. 1966). Infes• corns than of susceptible ones. tation counts for a 2-year period over five souther n While Heliothis spp probably do not cause U.S. states averaged 83% infested ears, but most severe yield losses in maize, the crop serves as the damage was indirect, as feeding by H. zea permit• source of infestation for other crops such as cotton, ted entrance of rice weevil and pink scavenger soybeans, and many vegetable crops. Therefore if larvae (Starks et al. 1966). The low injury level f r o m high levels of resistance did occur in maize, many H. zea is probably associated with the strong canni• other crops would benefit. balistic habits of the larvae, whereby only one larva Ortega et al. (1980) give a comprehensive per ear matures, regardless of the number of eggs review of Heliothis resistance in maize; however, deposited on the silk. no information is given on economic thresholds or Sweet corn is a high-value cash crop, and the value of the resistance sources in lowering field because of strong consumer preference, must be infestations. nearly worm-free. This condition requires high pes• Likewise, the review by Maxwell et al. (1972) lists ticide usage. Host-plant resistance cannot provide many references relating to Heliothis resistance in the protection that is demanded for sweet corn maize, but no attempt is made to appraise the value w h e r e Heliothis is an economic problem. of these characters in suppressing populations. Numerous citations in the literature report on sources of resistance to H. zea. Yarnell (1952) and Walter (1957) first reported on lines that possesse d Sorghum and Millet resistance to H. zea, however, these early studies lacked standards against which comparisons Sorghums are frequently attacked by H. zea but could be made. The investigators reported on a seldom receive insecticidal treatments for its con• lethal factor in the silk, but this proved to be elusive trol. It is generally recognized that the loose- when later investigators subjected it to rigorous headed varieties suffer less damage than those tests (Luckman et al. 1964; Knapp et al. 1967; with a compact head. Starks et al. 1967; Straub and Fairchild 1970). Man y Burkhardt (1957) found that two to three larvae of these studies were based on laboratory experi• per head were required to cause economic losses, ments where freeze-dried silks were incorporated while Kinzer and Henderson (1968) found that one into larval diet. Growth on diets containing both larva per head reduced yields by approximately susceptible and resistant silks was very poor. 4 % . Another resistant character that appears in the The only reference found pertaining to Heliothis literature is the long and tight husk of maize, whi c h resistance in sorghum was a laboratory study by has been reported by numerous investigators as a Oliver and Tipton (1972) who made a diet of mature resistance mechanism. Ditman and Cory (1933) seed. They noted wide differences between varie• reported that these characters reduced kernel ties; however, no attempt was made to correlate damage because larvae took longer to traverse the these studies with field observations. silk channels before reaching the kernels. Essen- Millet is also frequently attacked, though Helio-

2 2 7 this is not considered a major pest in millet. Burton Spanish types generally suffered greater damage et al. (1977) found that a trichomeless variety had than runner or Virginia types. 75 times fewer eggs than its isogenic hairy counterpart. Chickpea

Tobacco Heliothis spp can be very damaging to the chickpea crop in the Americas as well as in Asia. How- Tobacco is a high-value cash crop, and leaf dam• ever, no references noting differences in age lowers the grade and price of the crop. infestation or studies to identify resistance were Several workers have reported on tobacco spe• found. cies or cultivars that exhibit marked differences in response to H. virescens. Burk and Stewart (1971) surveyed the different Nicotiana species for resist- Host-Plant Resistance to Heliothis: a n c e to Heliothis and noted that a cultivar of N. An Appraisal tabacum had high levels of resistance to H. virescens. Greene and Thurston (1971) noted that H. Problems virescens showed a strong preference for tobacco with pubescent leaves over types with smooth Heliothis spp have a wide host range and are multi- leaves. However, Girardean et al. (1973) related H. generation pests. Therefore a population may build virescens damage of flue-cured tobacco to nico• up on one crop and then move to another in large tine content, trichome density, and exudates. They numbers. Since the population increase may not found that the more pubescent lines tended to occur within the crop as in monophagous pests, suffer less larval damage, as the trichomes high levels of resistance are required if populations impeded the movement of the larvae. are to be stabilized below the economic threshold level. The probability of finding a single mechanism that will provide this level of suppression is remote, Other Legumes and therefore several characters must be com• bined. While this is not an unrealistic approach, it Pigeon pea does require good methodology in order to recover lines that contain multiple sources of resistance. Heliothis spp are recognized as major pests of pigeonpea. In the Americas, pigeonpea is grown principally in the Caribbean Islands, where it is an Progress important food source. Cruz (1975) from Puerto Rico reported on some preliminary studies showing The literature documents that it is possible to locate that some lines had significantly fewer Heliothis plant characters that affect Heliothis growth and eggs deposited while others suffered less damage development in the major crops. Admittedly, many from larvae. of these references are based on laboratory exper• Davies and Lateef (1978) reported that in India iments, and field suppression has not been demon• certain pigeonpea lines have shown lower levels of strated, but differences do occur between cultivars pod damage from H. armigera, but no resistant and could be exploited. When research programs lines have been identified as yet. have received good support, progress has been demonstrated.

Groundnut Prospects In the Americas, H. zea can cause economic losses to groundnut. But only one reference to plant Progress in host-plant resistance research is a resistance could be located. Leuck et al. (1967) long-term proposition and requires considerable evaluated 14 varieties for insect damage using a resources. With the limited financial resources visual damage score. Ragging, principally due to H. available today, many host-plant resistance pro• zea, ranged from 1.65 to 3.92 on a scale of 1 to 5. jects have suffered; unfortunately, funding is avail-

2 2 8 able only w h e n a crisis is looming, a n d with t h e cultivars to bean leaf beetle, striped blister beetle, a n d availability of the synthetic pyrethroids, there is no bollworm. Journal of Economic Entomology 65(6):1669 - crisis on the horizon. An effective pesticide makes 1 6 7 2 .

control of the pests very easy and also insures CRUZ, C.1975. Observations on pod borer oviposition stability of yields. Very little management is and infestation of pigeon pea varieties. Journal of t h e required, and even if the number of applications is Agricultural University of Puerto Rico 59(1 ):63-68. excessive, the grower has minimized the risk at DAVIES, J.C., and LATEEF, S.S. 1978. Recent trends very little extra cost. Therefore in crops that have a in grain legume pest research in India. Pages 25-31 in low damage threshold, or that have a number of Pests of grain legumes: ecology and control, eds. S.R. different pest species, population suppression will Singh, H.F. van Emden, and T.A. Taylor. London, UK: probably rely on conventional pesticides. When IITA/Academic Press. pest resistance to the synthetic pyrethroids DEL VALLE.C.G., and MILLER, J.C. 1963. Influence of b e c o m e s w i d e s p r e a d , the d o s a g e s c a n b e husk length and tightness against corn earworm damag e markedly increased and still require only relatively in sweet corn. American Society of Horticultural Sc i e n c e s small amounts. Proceedings 83:531 -535. However, there are many crops where pesticide DITMAN, L.P., and CORY, E.N. 1933. Corn earworm use is not part of the production s y s t e m . T h e s e are studies. Maryland Agricultural Experiment Station Bulletin usually crops that have a low cash value per unit of 348:525-543 land or crops grown in regions where growers do DREYER, D.L., BINDER, R.G., CHAN, B.G., WAISS, not have access to chemicals or the equipment to A.C., HARTWIG, E.E., and BELAND, G.L. 1979. P i n - apply t h e m . It is in these situations that host-plant itol, a larval growth inhibitor for Heliothis zea in soybeans. resistance will have its potential impact. Experiment 35:1182-1183.

FERY, R.L., and CUTHBERT, F.P. 1973. F a c t o r s affecting evaluation of fruitworm resistance in toma t o . Journal of the American Society of Horticultural Sc i e n c e References 98(5):457-459.

BELAND, G.L., and HATCHETT, J.H. 1976. E x p r e s • FERY, R.L., and CUTHBERT, F.P. 1974. Resistance of sion of antibiosis to the bollworm in two soybean ge n o • tomato cultivars to the fruitworm. Horticultural Sc i e n c e types. Journal of Economic Entomology 6(4):557-560 9(5):469-470.

BIRD, L.S., ED-ZIK, K.M., FREE, E., and ARNOLD, R. FERY, R.L., and CUTHBERT, F.P. 1975. Antibiosis in 1 9 6 8 . Concepts and procedures for developing cottons Lycopersicon to the tomato fruitworm. Journal of the with multiple disease resistance. Pages 158-162 in Pro• American Society of Horticultural Science 100(3):27 6 - ceedings, Beltwide Cotton Producers Research Confer • 2 7 8 . ence, Cotton Disease Council 28. GALLUN, R.L., STARKS, K.J., and GUTHRIE, W.D. BURK, L.G., and STEWART, P.A. 1971. Survey of res• 1975. Plant resistance to insects attacking cereals. istance among Nicotiana spp. to tobacco budworm. Annual Review of Entomology 20:337-358. Tobacco Science 15:32-34. GlRARDEAN, J.H., GAINES, T.P. and GOLDEN B.A. BURKHARDT, C.C. 1957. Corn earworm control in 1973. Possible causes of differences in tobacco bud- grain sorghum. Journal of Economic Entomology worm damage to flue-cured tobacco varieties. Journal o f 50(4):539-541. Economic Entomology 66(2):470-472.

BURTON, G.W., HANNA, WW., JOHNSON, J.C., GRAY, JR., MABRY, T.J., BELL, A.A., STIPANOVIC, LEUCK, D.B., MONSON, W.G., POWELL, J.B., R.D., and LUKEFAHR, M.J. 1976. Para Hemigossypo- WELLS, H.D., and WIDSTROM, N.W. 1977. Pleiotropic lone: a requiterpenoid aldehyde quinone from Gossypium effects of trichomeless gene in pearl millet on tra n s p i r a • hirsutum. 1976 (3):109-110. tion, forage quality, and pest resistance. Crop Sci e n c e GREENE, G.L., and THURSTON, R. 1971. O p p o s i - 17:613-616. tional performance of Heliothis virescens a n d Nicotiana CHAN, B.G., WAISS, A.C., and LUKEFAHR, M.J. species. Journal of Economic Entomology 64(3): 641 - 1 9 7 8 . Condensed tannin, an antibiotic chemical from 6 4 3 . Gossypium hirsutum. Journal of Insect Physiology GUTHRIE, W.D., and WALTER, E.V. 1961. C o r n e a r - 24:113-118. worm and Egropean corn-borer resistance in sweet cor n CLARK, W.J., HARRIS, F.A., MAXWELL, F.G., and inbred lines. Journal of Economic Entomology HARTWIG, E.E. 1972. Resistance of certain soybean 54(6):1248-1250.

2 2 9 HEILMAN, M.D., LUKEFAHR, M.J., NAMKAN, L.W., HAM, N.M. 1971. Suppression of Heliothis populations and NORMAN, J.W. 1977. Field evaluation of a short with glabrous cotton strains. Journal of Economic E n t o • season production system in Lower Rio Grande Valley o f mology 64(2):486-488. Texas. Pages 80-82 i n Proceedings, Beltwide Cotton Pro• LUKEFAHR, M.J., HOUGHTALING, J.E., and ducers Research Conference, Dallas, Texas, USA. CRUMB, D.G. 1975. Suppression of Heliothis s p p . w i t h KENNEDY, G.G. 1978. Recent advances in insect res• cottons containing combinations of resistant charac t e r s istance of vegetables and fruit crops in North Amer i c a . Journal of Economic Entomology 68(6)743-746. Bulletin of Entomological Society of America 24:375 - 3 8 4 . MAXWELL, F.G., JENKINS, J.N., and PARROT, W.L. KINZER, H.G.,and HENDERSON, C.F. 1968. D a m a g e 1 9 7 2 . Resistance of plants to insects. Advances in by the larvae of the corn earworm to grain sorghum. Agronomy 24:187-265. Journal of Economic Entomology 61(2):263-267. MEYER, A.J., and MEYER, V.G. 1961. Origin and inher• KOGAN, J., SELL, D.K., STINNER, RE., BRADLEY, itances of nectariless cotton. Crop Science 1:167-169. J.R.,and KOGAN, M. 1978. V. A bibliography of Heliothis MUELLER, A. J., and ENGROFF, B.W. 1980. Effects of zea a n d H. virescens (Lepidoptera: Noctuidae). INTSOY infestation levels of Heliothis zea on soybeans. Journal of Series Number 17; University of Illinois, Urbana, III, U S A . Economic Entomology 73(2):271-275. 2 4 2 pp. OLIVER, B.F., and TIPTON, K.W. 1972. Effect of diet KNAPP, J.L., HEDIN, P.A., and DOUGLAS, W.A. formulated from sorghum hybrids on weight gain of cor n 1 9 6 5 . Amino acids and reducing sugars in silks of corn earworm larvae. Journal of Economic Entomology resistant or susceptible to corn earworm. Annals of t h e 65(5):1759-1760. Entomological Society of America 58(3):401 -402 ORTEGA, A., VASAL, S.K., MIHM, J., and HERSHEY, KNAPP, J.L., MAXWELL, F.G., and DOUGLAS, W.A. C. 1980. Breeding for insect resistance in maize. In 1 9 6 7 . Possible mechanisms of resistance of dent corn to Breeding plants resistant to insects, eds F.G. Maxw e l l the corn earworm. Journal of Economic Entomology and P.R. Jennings. New York, USA: Wiley. 60(1):33-35. PARNELL, F.R., KING, H.E., and RUSTON, F.F. LANGE, W.T., and BRONSON, L. 1981. Insect pests of 1 9 4 9 . Jassid resistance and hairiness of the cotton plant. tomato. Annual Review of Entomology 26:345-371. Bulletin of Entomological Research 39:539-575. LEUCK, D.B., HAMMOND, R.O., MORGAN, L.W., and PEARSON, O.E. 1959. The insect pests of cotton in HARVEY, J.E. 1967. Insect preference for peanut varie• tropical Africa. London and Reading, UK: Eastern Press. ties. Journal of Economic Entomology 60(6):1546-154 9 . SCHUSTER, M.F., LUKEFAHR, M.J., and MAXWELL, LOWRY, W.L. 1966. Bollworm and tobacco budworm F . M . I 9 7 6 . Impact of nectariless cotton on plant bugs and resistance to some insecticides in the Lower Rio Gr a n d e natural enemies. Journal of Economic Entomology Valley in 1964. Journal of Economic Entomology 59 69(3):400-402. (2):479-480. SCHUSTER, M.F., 1980. New sources of high tannin LUCKMAN, W.H., RHODES, A.M., and WANN, E.V. resistance to Heliothis in upland cotton resulting in feed• 1964. Silk balling and other factors associated with res • ing deterrance Pages 126-129 in Proceedings, Beltwide istance to the corn earworm. Journal of Economic En t o • Cotton Producers' Research Conference, New Orleans, mology 57(5):778-779. La. U S A . LUKEFAHR, M.J., BOTTGER, G.T., and MAXWELL, STARKS, K.J., COX, H.C., McMILLIAN, W.W., and F . G . 1 9 6 6 . Utilization of gossypol as a source of insect BURTON, R.L. 1966. Damage to corn by the pink sca• resistance. Pages 215-222 i n Proceedings, Beltwide Cot• venger caterpillar and its relationship to earworm a n d rice ton Producers' Research Conference, Memphis, Tenn, weevil damage. Journal of Economic Entomology USA. 60(4):920-923. LUKEFAHR, M.J., and MARTIN, D.F., 1964. T h e STRAUB, R.W., and FAIRCHILD, M.L. 1970. L a b o r a • effects of various larval and adult diets on the fe c u n d i t y tory studies of resistance in corn to the corn earw o r m . and longevity of the bollworm.tobacco budworm and co t • Journal of Economic Entomology 63(6):1901-1903. ton leafworm. Journal of Economic Entomology 57(2): 2 3 3 - 2 3 5 . STIPANOVIC, R.D., BELL, A.A., O'BRIEN, D.H., and

LUKEFAHR, M.J., COWAN, C.B., PFRIMMER, LUKEFAHR, M.J. 1977. Heliocide H2: an insecticidal 2 T.R.,and NOBLE, L.W. 1966. Resistance of experimen• sesterterpenoid from cotton (Gossypium) . Tetrahedron tal cotton strain 1514 to the bollworm and cotton fl e a - Letter 6:567-570. hopper. Journal of Economic Entomology 59(2):393-39 5 . TURNIPSEED, S.G., and KOGAN, M. 1976. S o y b e a n LUKEFAHR, M.J., HOUGHTALING, J.E., and GRA- entomology. Annual Review of Entomology 21:247-282.

2 3 0 WALKER, J.K., Jr., and NILES, G.A. 1971. Population dynamics of the boll weevil and modified cotton typ e s . Texas Agricultural Experiment Station Bulletin 1109 , U n i • versity Station, Tex, USA.

WALTER, E.V. 1957. Corn earworm lethal factor in silks of sweet corn. Journal of Economic Entomology 50(1):105-106.

WISEMAN, B.R., McMILLIAN, W.W., and WID- STROM.N.W. 1970. Husk and kernel resistance among maize hybrids to an insect complex. Journal of Econ o m i c Entomology 63(4): 1260-1262.

WOLFENBARGER, D.A., LUKEFAHR, M.J., and GRA• HAM, H.M. 1971. A field population of bollworms resist• ant to methyl parathion. Journal of Economic Entomo l o g y 64(3)755-756.

YARNELL, S.H. 1952. Breeding for resistance to the corn earworm in sweet corn. Proceedings, Association o f Southern Agricultural Workers 49:106-107.

ZUBER, M.S., FAIRCH1LD, M.L., KEASTER, A.J., and FERGUSON. V.L. 1971. Evaluation of 10 generations of mass selection for corn earworm resistance. Crop Science 11:16-18

231

The Potential Role of Natural Product Chemistry Research in Heliothis Management

Martin Jacobson*

Abstract

The chemistry and potential applications of naturally occurring toxicants, repellents, feeding deterrents, growth and mating inhibitors, and sex pheromones lor controlling Heliothis zea, H. virescens, and H. armigera are reviewed. The sex pheromones of the respective species are useful tor surveying areas of infestation, as mass-trapping agents, and as mating suppressants through the contusion technique. The use of various types of traps and pheromone dispensers is compared. Confusion agents such as (Z)-9-tetradecen-l-ol formate are potentially valuable tor the suppression of mating. Feeding deterrents obtained from plants promise to be useful alone as well as in integrated pest-management programs against the pest species of Heliothis.

In the United States, Heliothis zea (Boddie), com• repellents, (2) feeding deterrents, and (3) sex monly called the bollworm, corn earworm, or pheromones. I will treat these separately, dealing tomato fruitworm, and H. virescens (F.), commonly only with the more recent significant developments known as the tobacco budworm, are generally now in use or potentially useful. referred to as the "bollworm complex." Both species feed on a wide range of host plants, and a free exchange of hosts occurs between cotton and Toxicants and Repellents other host plants. H. armigera (Hubner), the Old World bollworm, is an important crop pest in many Host-plant resistance has been recognized since areas of Africa, the Near and Middle East, Asia, an d the early 1800s. From the standpoint of natural Australia. Although H. zea was long believed to be selection in evolution, resistance is a preadaptive identical with H. armigera, the two are now recog• characteristic of plants. Before being cultivated by nized as distinct species (Balachowsky 1972). man, plants, coevolving with insects, either intrinsi• Natural substances have proved to be extremely cally possessed or have developed means of sur• valuable for surveying areas of infestation as- well viving attack by arthropods. as in the control of these highly destructive crop Normal commercial cottons have 3000 to 5000 pests. These substances are: (1) toxicants and trichomes per square inch (465 to 775/cm2 ) on the leaves present on the growing points of the plant. Years ago it was suggested that the presence of *U.S. Department of Agriculture, Agricultural Research Service. dark internal glands in cotton (Gossypium) plants Biologically Active Natural Products Laboratory, Beltsville, Md, USA. was associated with resistance to insects, and

International Crops Research Institute tor the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. gossypol isolated from these glands was consi• tree, Melia azedarach L, which is native to the dered to be the main contributing factor against United States as well as India, resulted in only slight tobacco budworm, H. virescens ( s e e W a i s s et al. feeding, gross reduction in growth, and high mortal• 1977, and Maxwell 1977 for comprehensive ity (McMillian et al. 1969). The results were identi• reviews of the subject). However, a glandless res• cal when last-instar larvae of H. virescens w e r e istant variety was developed that contains no gos• offered a diet containing the well-known antifee- sypol, and a condensed tannin (p-hemigossypolone)) dant azadirachtin, isolated from the seeds of the was identified as the resistance factor (Gray et al. Indian neem tree, Azadirachta indica A. Juss. (Rus- 1976). Addition of cotton tannin at 0.1 to 0.3% to a c o e 1972). synthetic diet markedly reduces the weight of lar• Phenylacetaldehyde, a compound found in vae reared on the diet. A number of sesterterpe- many plants and available at low cost on the open noids have also been isolated from cotton market, attracts large numbers of adult H. zea flowerbuds that are highly toxic to H. zea a n d H. (mainly females) to field traps (Cantelo and Jacob- virescens (Stipanovic et al. 1977, 1978a, 1978b); son 1979). A microencapsulated formulation of they have been designated "heliocides H1 , H2 , H3 , phenylacetaldehyde caused a reduction in the H4," and can be synthesized by a Diels-Alder reac- number of eggs laid as well as the amount of dam• tion between hemigossypolone and frans-3 age done to cotton plant terminals (Flint et al. 1978). ocimene. It is suggested that plant breeders select This compound also attracts many other species of for cotton plants with higher pigment content as a lepidopterous insects, especially when used in mechanism of resistance (Schuster 1979). black-light traps. In laboratory tests, Ignoffo et al. (1981) showed that incorporation into the diet of either of two varie• ties of Bacillus thuringiensis was lethal to larvae of Sex Pheromones H. zea a n d H. virescens. The LC50 values with variety israelensis were 19.3 and 27.6 µg/ml, Heliothis armigera respectively; with variety kurstaki, 2.0 and 7.8 µ g / m l , respectively. The composition of the female sex pheromone A toxic factor that kills H. zea larvae feeding on appears to vary with the location in which the wild tomato, Lycopersicon hirsutum f. glabratum insects are found. Piccardi et al. (1977) isolated CM. Mull., has recently been identified as 2- (Z)-11 -hexadecenal from abdominal tips of Suda• tridecanone (Williams et al. 1980). It is also toxic to n e s e H. armigera females, and this compound several other species of insects. alone was attractive to males in field traps. How• ever, Dunkelblum et al. (1980a, 1980b) found both (Z)-11-hexadecenal and (Z)-9-hexadecenal, in a Feeding Deterrents and ratio of 30:1, in tip extracts of females from Israel, Growth Inhibitors and these did not attract males unless they were combined (Kehat et al. 1980). Working with Florets of the sunflower, Helianthus annuus L., extracts from the abdominal tips of females reared have yielded two diterpene acids, trachyloban-19- from pupae in Botswana, Sudan, India, and Malawi, oic acid and the biogenetically related (-)-16- Nesbitt et al. (1979) isolated and identified (Z)-11 - kauren-19-oic acid, that drastically reduce larval hexadecenal and (Z)-11-hexadecen-1-ol, plus a g r o w t h of H. zea a n d H. virescens when incorpo• third component, (Z)-9-hexadecenal, which rated in t h e diet (Elliger et al. 1976). occurred only in females originating in Malawi. A Severe retardants of larval growth for H. zea have reexamination of the pheromone components by been isolated from corn silk; they are the glycosidal these investigators (Nesbitt et al. 1980) using ovi• flavones maysin (Waiss et al. 1979) and 211-O-L- positor washes showed that (Z)-11 -hexadecenal rhamnosy l - 6 - C - (6-deoxyxylo - hexos - 4 - ulosyl) luteo- and (Z)-9-hexadecenal were consistently present lin(Elliger et al. 1980b). Results obtained by testing in moths from all of these origins in the ratio of a variety of plant flavonoids as retardants of growth 88.6:2.9. a n d d e v e l o p m e n t for H. zea are given by Elliger et Field tests conducted in Israel by Kehat et al. al. (1980a). (1980) showed that traps baited with (Z)-11- Offering first-instar H. zea larvae a diet contain• hexadecenal containing 1 to 10% (Z)-9- ing a chloroform extract of leaves of the chinaberry hexadecenal caught more male moths than traps

2 3 4 baited with (Z)-11 -hexadecenal alone. Addition of hexadecenal and 2.25 µg (Z)-9-hexadecenal are (Z)-11 -hexadecen-1 -ol reduced the catches. quite effective for attracting male moths into baited There is no doubt that the two aldehydes are traps. essential components of the sex pheromone. The mixture of (Z)-11-hexadecenal and (Z)-9- hexadecenal, in the ratio of 97:3, is currently in use Mating Inhibitors in Israel for monitoring H. armigera populations (Dunkelblum et al. 1980a). A considerable amount of recent research has demonstrated that pheromonal communication between the sexes of a number of species of Lepi- Heliothis virescens doptera can be effectively disrupted by permeating the air with synthetic compounds identical with or The sex pheromone produced and released by the similar to the true pheromones of the target species adult female was identified by Roelofs et al. (1974) (see especially Roelofs 1977 and Mitchell 1981). and Tumlinson et al. (1975) as a blend of (Z)-11- In field tests conducted in Florida, evaporation of hexadecenal and (Z)-9-tetradecenal; it has been (Z)-11-hexadecenal (a component of Heliothis named "virelure." The natural ratios of these com• pheromones) reduced the mating of H. zea f e m a l e s ponents were found by Roelofs et al. to be 3:1 in the by 85%. Evaporation of (Z)-9-tetradecenal (a com• abdominal tips of females one-half to 4 days old, ponent of the H. virescens pheromone) did not and by Tumlinson et al. to be about 16:1 in an ether affect H. zea behavior but did reduce the mating of wash of whole females. H. virescens females by 95% (Mitchell et al. 1976). In 1980, Klun et al. (1980a) reported that heptane In 1975, (Z)-9-tetradecen-1-ol formate, a com- washes of female ovipositors yielded 77 to 91% pound of nonbiological origin but closely related (Z)-11 -hexadecenal, 1 to 3% (Z)-9-tetradecenal, structurally to (Z)-9-tetradecenal, was found to be 0.1 to 2.0% (Z)-7-hexadecenal, 0.3 to 2.0% (Z)-9- an excellent disruptant of pheromonal communi• hexadecenal, 3 to 19% hexadecanal, 1 to 5% (Z)- cation between male and female corn earworms 11 -hexadecen-1 -ol, and 1 to 3% tetradecanal. In and between male and female tobacco budworms field bioassays, a 152 µg mixture of these seven when it was evaporated into the air of infested fields compounds deployed in an insect trap was five to (Mitchell et al. 1975). The use of this compound for six times more attractive than virelure alone. this purpose has been patented in the United Neither of the two components of virelure alone States (Mitchell et al. 1978). Capture of the moths will attract male moths in the field. by pheromone traps in fields in which the formate was released from vials was reduced by more than 95% for both H. zea a n d H. virescens. T h e c o m - Heliothis zea pound, which is easily prepared, highly stable, and safe for use, was mentioned by Bestmann et al. Although the presence of a sex attractant in an (1975) as occurring naturally in an extract of extract of virgin female abdominal segments was female H. virescens abdomens, but this claim was first demonstrated in 1965 by Bergeretal. (1965), it later rescinded by these investigators in personal was not until 1970 that two discrete components correspondence with me. were isolated by McDonough et al. (1970). How• Gothilf et al. (1978) reported that (Z) - 9 - ever, the latter investigators could obtain only par• tetradecen - 1 - ol formate and (Z) - 9 - t e t r a d e c e n - 1 -ol tial identification of these compounds, which they acetate released from virgin female-baited traps in reported to be a 14-carbon straight-chain alcohol the field were equally effective in inhibiting male and a 14-carbon acetate. capture of H. armigera. In 1980, Klun et al. (1980a, 1980b, 1980c, 1980d) Slow release of the formate from laminated Her- reported the isolation and identification of the co m • ••• plastic dispensers in a corn field was very ponents of the natural pheromonal blend obtained effective in reducing mating by H. zea in 1977 (Caro from heptane washes of virgin female ovipositors. et al. 1980). The compound is normally dispensed The composition consisted of 90 to 95% (Z)-11 - from microcapsules, plastic laminates, or hollow hexadecenal, 1 to 2% (Z)-9-hexadecenal, 0.4 to fibers. 2.0% (Z)-7-hexadecenal, and 2 to 7% hexade- A sensitive method for determining the formate in canal. Binary mixtures containing 11 5µ g (Z)-11- air was developed by Caro et al. (1979).

2 3 5 Application (Trap Types vaporization and oxidation of virelure (Hendricks et and Dispensers) al. 1977). Hollingsworth et al. (1978) compared the catches of electric grid traps of several types and Heliothis armigera nonelectric traps, all of which were baited with virelure. Standard and modified grid traps outper• The use of dental roll dispensers impregnated with formed miniature grid traps, but a wire mesh cone synthetic pheromone was not as effective as trap with no bottom was far superior to any of the rubber dispensers in plastic pail-type traps in Israel other nonelectric traps. (Gothilf et al. 1979). Rubber dispensers are cur• Rubber septa baited with virelure caught as rently in use in cotton fields throughout Israel for many males as did live females when used in cone survey purposes (Gothilf et al. 1981), using 2 mg of traps and were effective for 10 weeks. Laminated a 97:3 mixture of (Z)-11 -hexadecenal and (Z)-9- baits used for comparison were effective for only 3 hexadecenal plus 0.2 mg of an antioxidant. This weeks, with decreasing effectiveness for 2 more mixture is effective from rubber dispensers but not weeks (Flint et al. 1979). from polyethylene vials (Kehat et al. 1980). Hartstack et al. (1979) reported an efficiency of Using traps made of two plastic rectangles about 25% for capturing males in a nonelectric joined at each corner by rings, with the inner sur• cone trap. This trap can be baited with virelure or face of the bottom rectangle coated with adhesive, live females and is portable, inexpensive, and sim• a small rubber capsule saturated with (Z)-11- ple to install and operate. hexadecenal was very effective in capturing male Sparks et al. (1979b) field-tested virelure in moths in Senegal (Bourdouxhe 1980). cigarette filters and live females in Georgia and Arizona using standard electrocutor grid traps, pie- plate sticky traps, wind-vane traps, and skirted Heliothis virescens cone-type traps. The grid traps proved to be most efficient and the pie-plate traps were least efficient.

Comparative tests conducted with virelure in In tests comparing the efficiency of a wind- unpainted vs. painted paper icecream carton traps oriented trap with pie-plate and grid traps, all of showed that fluorescent orange, green, tangerine, which were baited with live females or virelure, the and highly reflective white were much superior to wind-oriented trap was almost as efficient as the unpainted traps. Green appeared to be best for grid trap and more efficient than the nonelectric monitoring and mass-trapping (Hendricks et al. traps (Raulston et al. 1980). This trap was also very 1972). efficient for capturing male H. zea when it was baited with live H. zea females. In the U.S. Virgin Islands, electric grid traps baited with live virgin females captured 101 times Inverted single-cone traps baited with live more males than did unbaited black-light traps and females captured more males at night during peri• 9 times more than sticky cardboard traps baited ods of low wind velocity (0-9.6 km/hr) and wind- with females (Goodenough and Snow 1973). vane traps captured more males at higher wind Placement of the bait inside the grid element was velocities (9.6-16 km/hr) (Hendricks et al. 1980). more effective than placement about 15 cm to one side of the element. Saucer-type female-baited traps placed 1.5 m above the ground (just above Heliothis zea the top of the cotton vegetation) caught signifi• cantly more males than those placed higher or Grid traps baited with a mixture of (Z)-9- lower (Hendricks and Leal 1973). hexadecenal were much more efficient for captur• Virelure (10 mg) laminated between thin sheets ing males than a baited wind-vane trap; a baited of vinyl polymer plastic attracted males to baited sticky pie-plate was worst of all (Sparks et al. traps for at least 21 days. A mixture of 10 µI of 1979a). (Z)-11-hexadecenal and 0.5 µI of (Z)-9- Grid traps baited with live female H. subflexa tetradecenal was attractive for at least 5 days whe n ( G u e n e e ) , H. virescens, or H. zea captured con- incorporated in a 8 x 30 mm cigarette filter encase d specific males with few exceptions. Simultaneous in a glass shell vial. Cottonseed oil and polyethy• use of H. subflexa females with females of either of lene glycol 600 distearate inhibited the excessive the other two species resulted in lower catches of

2 3 6 males of either species. Exposure of laboratory- B E S T M A N N , H . J . , S T R A N S K Y , W . , V O S T R O W S K Y , reared male H. virescens or male H. subflexa to O . , and R A N G E , P . 1975. P h e r o m o n e , VII. S y n t h e s e v o n virelure in a Plexiglas wind tunnel showed that only 1 -substituierten ( Z ) - 9 - A l k e n e n . C h e m i s c h e B e r i c h t e 108: 3 5 8 2 - 3 5 9 5 . H. virescens responded (Tingle et al. 1978). B O U R D U X H E , L. 1980. Study of c h a n g e s in Heliothis armigera flights with synthetic pheromone traps in Sene• Conclusions gal. T r o p i c a l Pest M a n a g e m e n t 2 6 : 1 0 7 - 1 0 9 . C A N T E L O , W . W . , a n d J A C O B S O N , M . 1 9 7 9 . P h e n y l - In addition to using the respective sex pheromones acetaldehyde attracts moths to bladder flower and to of Heliothis species for essential monitoring of blacklight traps. Environmental Entomology 8: 444-447. infested areas, these compounds have been C A R O , J . H . , F R E E M A N , H . P . , a n d B I E R L - shown to be useful as mass-trapping agents as L E O N H A R D T , B.A. 1979. D e t e r m i n a t i o n o f ( Z ) - 9 - well as for mating suppression through confusion. t e t r a d e c e n - 1 - o f f o r m a t e , a Heliothis s p p . m a t i n g The use of rubber dispensers in green traps is disruptant, in air by electron-capture gas chromato• recommended, especially with H. virescens, for graphy following photolytic cleanup. Journal of Agricu l t u • survey, and electric grid traps baited with live ral a n d Food C h e m i s t r y 2 7 : 1 2 1 1 - 1 2 1 5 . females or the sex pheromone appear to be more C A R O , J . H . , G L O T F E L T Y , D.E., and F R E E M A N , H . P . efficient for mass-trapping than black-light traps. 1 9 8 0 . (Z)-9-Tetradecen-1 -ol formate Distribution and Several types of cone traps, which are portable, dissipation in the air within a c o r n c r o p after e m i s s i o n f r o m lightweight, and inexpensive, are well-suited for a controlled-release formulation. Journal of Chemical use in areas where sources of electric power are E c o l o g y 6: 2 2 9 - 2 3 9 . not readily available in or near crop sites. Cigarette D U N K E L B L U M , E., G O T H I L F , S . , and K E H A T , M . filters and laminated sheets of vinyl polymer plastic 1980a. Identification of the sex p h e r o m o n e of the c o t t o n can also be recommended as pheromone dis• b o l l w o r m , Heliothis armigera, in Israel. P h y t o p a r a s i t i c a 8: pensers for slow release. 2 0 9 - 2 1 1 . Mating suppression through the use of confu- D U N K E L B L U M , E., G O T H I L F , S., and K E H A T , M . sants such as (Z)-9-tetradecen-1 -of formate for air 1980b. Identification of sex pheromones from Heliothis permeation is a potentially valuable development. It armigera, Spodoptera littoralis a n d Plusia chalcites. P h y - has been shown to be very effective with H. zea a n d l o p a r a s i t i c a 9:77. H. virescens, which are serious pests in highly E L L I G E R . C.A., Z I N K E L , D.F., C H A N , B.G., a n d diverse American ecosystems, and should cer• W A I S S , A . C . , Jr. 1976. Diterpene acids as larval growth tainly be pursued for the same purpose with H. inhibitors. Expenentia 32: 1 3 6 4 - 1 3 6 6 . armigera. E L L I G E R , C.A., C H A N , B.G., and W A I S S , A . C . , Jr. A promising ovipositional inhibitor, phenylacetal- 1980a. Flavonoids as larval growth inhibitors. Naturwis- dehyde, has been shown to be effective for H. zea s e n s c h a f t e n 67: 3 5 8 - 3 6 0 . and should be tried for other species of Heliothis as a contact spray of dust formulation as well as E L L I G E R , C.A., C H A N , B.G., W A I S S , A . C . , Jr. L U N - through slow release. D I N , R . E . , a n d H A D D O N , W . F . 1 9 8 0 b . C - Glycosylflavones from Zea mays that inhibit i n s e c t Broad-spectrum feeding deterrents such as development. Phytochemistry 19:293-297. extracts or isolates of chinaberry leaves and neem seeds, as well as the more selective gossypol and F L I N T , H . M . , N O B L E . J . M . , and S H A W , D . 1978. P h e - cotton heliocides, are potentially useful alone and nylacetaldehyde: tests for control of the pink bollworm in programs of integrated pest management of a n d o b s e r v a t i o n s o n other L e p i d o p t e r a infesting c o t t o n . Journal of the Georgia Entomological Society 13:284- Heliothis. 2 8 9 .

F L I N T , H . M . , N O B L E , J . M . , S A L T E R , S.S., and W A L • T E R S , S. 1979. R u b b e r septa: a l o n g - l a s t i n g s u b s t r a t e References for (Z)-11 - h e x a d e c e n a l a n d ( Z ) - 9 - t e t r a d e c e n a l , t h e p r i m • ary c o m p o n e n t s of the sex p h e r o m o n e of t h e t o b a c c o B A L A C H O W S K Y , A . S . 1972. E n t o m o l o g i e a p p l i q u e a budworm. Journal of Economic Entomology 72:798-800. l'agriculture, vol. 2. Paris: M a s s o n . G O O D E N O U G H , J . L . , a n d S N O W . J . W . 1 9 7 3 . B E R G E R , R.S., M c G O U G H , J . M . , a n d M A R T I N , D . F . Increased collection of tobacco budworm by electric 1965 . Sex attractants of Heliothis zea a n d H. virescens. grid traps as compared with blacklight and sticky traps . Journal of Economic Entomology 58: 1023-1024. Journal of Economic Entomology 66:450-453.

2 3 7 G O T H I L F , S . , K E H A T , M . , J A C O B S O N , M . , and K L U N , J.A., B I E R L - L E O N H A R D T , B.A., P L I M M E R , G A L U N , R . 1 9 7 8 . Screening pheromone analogues by J.R., S P A R K S , A . N . , P R I M I A N I , M . , C H A P M A N , O . L . , EAG technique for biological activity on males of Earias L E P O N E , G . , a n d L E E , G . H . 1 9 8 0 a . Sex pheromone insulana, Helolhis armigera, a n d Spodoptera littoralis. c h e m i s t r y o f t h e f e m a l e t o b a c c o b u d w o r m m o t h , Heliothis Environmental Entomology 7:31 -35. virescens. Journal of Chemical Ecology 6:177-183.

G O T H I L F , S., K E H A T , M . , D U N K E L B L U M , E., and K L U N , J.A., P L I M M E R , J.R., B I E R L - L E O N H A R D T , J A C O B S O N , M . 1 9 7 9 . Efficacy of (Z)-11 -tetradecenal B . A . , S P A R K S , A . N . , a n d C H A P M A N , O . L . as sex attractants for Heliothis armigera on t w o different 1 9 8 0 b . T r a c e c h e m i c a l s , t h e e s s e n c e o f s e x u a l c o m • dispensers. Journal of Economic Entomology 72:718- munication systems in Heliothis s p e c i e s . S c i e n c e 2 0 4 : 7 2 0 . 1 3 2 8 - 1 3 3 0 .

G O T H I L F , S . , K E H A T , M . , and D U N K E L B L U M , E . K L U N , J.A., P L I M M E R , J.R., B I E R L - L E O N H A R D T , 1 9 8 1 . Sex pheromones for monitoring populations of B.A., S P A R K S , A . N . , P R I M I A N I , M . , C H A P M A N , O . L . , Heliothis armigera. Phytoparasitica 9:78-79. L E E , G . H . , a n d L E P O N E , G . 1 9 8 0 c . Sex pheromone c h e m i s t r y of f e m a l e c o r n e a r w o r m m o t h , Heliothis zea. G R A Y , J.R., N A B R Y , T . J . , B E L L , A . A . , S T I P A N O V I C , Journal of Chemical Ecology 6:165-175. R . D . , a n d L U K E F A H R , M . J . 1 9 7 6 . P a r a - hemigossypolone: a sesquiterpenoid aldehyde quinone K L U N , J.A., P L I M M E R , J R . , S P A R K S , A . N . , and f r o m Gossypium hirsutum. Journal of the Chemical B I E R L - L E O N H A R D T , B.A. 1 9 8 0 d . Sex a t t r a c t a n t for Society, Chemical Communications 109-110. c o r n e a r w o r m m o t h s . U.S. Patent 4 , 2 1 6 , 2 0 2 . ( 5 A u g 1 9 8 0 ) . 4 p p . H A R T S T A C K , A . W . , W I T Z , J.A., and B U C K , D.R. 1 9 7 9 . M o t h t r a p s for the t o b a c c o b u d w o r m . J o u r n a l o f M A X W E L L , F . G . 1 9 7 7 . Plant r e s i s t a n c e t o c o t t o n Economic Entomology 72:519-522. i n s e c t s . Bulletin of t h e E n t o m o l o g i c a l S o c i e t y of A m e r i c a 23:199-203. H E N D R I C K S , D.E., H O L L I N G S W O R T H , J . P . , and H A R T S T A C K , A . W . , Jr. 1 9 7 2 . C a t c h o f t o b a c c o b u d - M c D O N O U G H , L . M . , G E O R G E , D.A., and L A N D I S , w o r m m o t h s i n f l u e n c e d b y c o l o r o f s e x - l u r e traps. Envir• B.J. 1 9 7 0 . Partial s t r u c t u r e of t w o sex p h e r o m o n e s of t h e onmental Entomology 1:48-51. c o r n e a r w o r m , Heliothis zea. Journal of Economic Ento• mology 63:408-412. H E N D R I C K S , D.E., a n d L E A L , M . P . 1 9 7 3 . C a t c h o f adult t o b a c c o b u d w o r m s i n f l u e n c e d b y height o f s e x - l u r e M c M I L L I A N , W . W . , B O W M A N , M . C . , B U R T O N , R.L., traps. Journal of Economic Entomology 66:1218-1219. S T A R K S , K.J., and W I S E M A N , B.R. 1 9 6 9 . Extract o f c h i n a b e r r y leaf as a f e e d i n g deterrent a n d g r o w t h r e t a r d - H E N D R I C K S , D . E . , H A R T S T A C K , A . W . , a n d ant for l a r v a e o f t h e c o r n e a r w o r m a n d fall a r m y w o r m . S H A V E R , T . N . 1 9 7 7 . Effect o f f o r m u l a t i o n s a n d d i s • Journal of Economic Entomology 62:708-710. p e n s e r s o n a t t r a c t i v e n e s s o f v i r e l u r e t o t h e t o b a c c o b u d - worm. Journal of Chemical Ecology 3:497-506. M I T C H E L L , E.R. 1 9 8 1 . M a n a g e m e n t o f i n s e c t p e s t s w i t h s e m i o c h e m i c a l s . N e w York, USA: P l e n u m Press. H E N D R I C K S , D . E . , P E R E Z , C . T . , and G U E R R A , R.J. 1 9 8 0 . Effects o f n o c t u r n a l w i n d o n p e r f o r m a n c e o f t w o M I T C H E L L , E.R., J A C O B S O N , M . , and B A U M - sex pheromone traps for noctuid moths. Environmental H O V E R , A . H . 1 9 7 5 . Heliothis spp.: d i s r u p t i o n of p h e r o m - Entomology 9:483-485. o n a l c o m m u n i c a t i o n with (Z) - 9 - t e t r a d e c e n - 1 - of f o r m a t e . Environmental Entomology 4:577-579. H O L L I N G S W O R T H , J . P . , H A R T S T A C K , A . W . , M I T C H E L L , E.R., B A U M H O V E R , A . H . , a n d J A C O B - B U C K , D.R., a n d H E N D R I C K S , D . E . 1 9 7 8 . Electric and S O N , M . 1 9 7 6 . R e d u c t i o n o f m a t i n g potential o f m a l e nonelectric moth traps baited with the synthetic sex Heliothis s p p . a n d Spodoptera frugiperda in field plots p h e r o m o n e o f t h e t o b a c c o b u d w o r m . U.S. D e p a r t m e n t o f treated with disruptants. Environmental Entomology A g r i c u l t u r e A R S - S - 1 7 3 , W a s h i n g t o n , D C , U S A . 5 : 4 8 4 - 4 8 6 .

I G N O F F O , C M . , C O U C H , T . L . , G A R C I A , C . , a n d M I T C H E L L , E.R., J A C O B S O N , M . , and B A U M - K R O H A , M . J . 1 9 8 1 . Relative activity of Bacillus thurin- H O V E R , A . H . 1 9 7 8 . (Z) - 9 - T e t r a d e c e n - 1 - ol f o r m a t e a n d giensis var. kurstaki a n d S. thuringiensis var. israelensis its u s e as c o m m u n i c a t i o n d i s r u p t a n t for Heliothis. U.S. a g a i n s t l a r v a e of Aedes aegypti, Culex quinquelasciatus, Patent 4 , 0 8 3 , 9 9 5 (11 A p r 1 9 7 8 ) 4 pp. Trichoplusia ni, Heliothis zea, a n d Heliothis virescens. Journal of Economic Entomology 74:218-222. N E S B I T T , B.F., B E E V O R , P.S., H A L L , D R . , and L E S - T E R , R . 1 9 7 9 . Female sex pheromone components of K E H A T , M . , G O T H I L F , S . , D U N K E L B L U M , E., a n d t h e c o t t o n b o l l w o r m , Heliothis armigera. J o u r n a l of I n s e c t G R E E N B E R G , S . 1 9 8 0 . Field e v a l u a t i o n o f f e m a l e s e x Physiology 25.535-541. p h e r o m o n e c o m p o n e n t s of t h e c o t t o n b o l l w o r m , Heliothis armigera. Entomologia Experimentalis et Applicata N E S B I T T , B.F., B E E V O R , P.S., H A L L , D.R., and L E S - 27:188-193. T E R , R . 1 9 8 0 . (Z) - 9 - h e x a d e c e n a l : a m i n o r c o m p o n e n t of

2 3 8 the female sex pheromone of Heliothis armigera ( H u b n e r ) TUMLINSON, J.H., HENDRICKS, D.E., MITCHELL, (Lepidoptera, Noctuidae). Entomologia Experimentali s e t E.R., DOOLITTLE, R.E., and BRENNAN, MM. Applicata 27:306-308. 1975 . Isolation, identification, and synthesis of the se x pheromone of the tobacco budworm. Journal of Chemic a l PICCARDI, P., CAPIZZI, A., CASSANI, G., SPINELLI, Ecology 1:203-214. P., ARSURA, E., and MASSARDO, P. 1977. A sex pheromone component of the Old World bollworm H e l i o - WAISS, A.C., Jr., CHAN, B.G., and ELLIGER, C.A. this armigera. Journal of Insect Physiology 23:1443-1445. 1 9 7 7 . Host plant resistance to insects. Pages 117-121 in Host plant resistance to pests, ed. PA Hedin, ACS Sym • RAULSTON, J.R., SPARKS, A.N., and LINGREN, P.D. posium Series 62, American Chemical Society, USA. 1 9 8 0 . Design and comparative efficiency of a wind- oriented trap for capturing live Heliothis spp Journal of WAISS, A C , Jr., CHAN, B.G., ELLIGER, C.A., WISE- Economic Entomology 73:586-589. MAN, B.R., McMILLIAN, W.W., WIDSTROM, N.W., 2UBER, M.S., and KEASTER, A.J. 1979. Maysin, a fla- ROELOFS, W.L. 1977. An overview—the evolving phil• vone glycoside from corn silks with antibiotic activity osophies and methodologies of pheromone chemistry. toward corn earworm. Journal of Economic Entomology Pages 287-297 in Chemical control of insect behavior: 72:256-258. theory and application, eds. H.H. Shorey and J.J. M c K e l - vey, Jr. New York, USA: Wiley-lnterscience WILLIAMS, W.G., KENNEDY, G.G., YAMAMOTO, R.T., THACKER, J.D., and BORDNER, J. 1980. 2 - ROELOFS, W.L., HILL, A.S., CARDE, R.T., and Tridecanone: a naturally occurring insecticide from t h e BAKER, T.C. 1974. Two sex pheromone components of wild tomato Lycopersicon hirsutum f. glabratum. S c i e n c e the tobacco budworm moth, Heliothis virescens. Life 207:888-889. Science 14:1555-1562.

RUSCOE, C.N.E. 1972. Growth disruption effects of an insect antifeedant. Nature 236: 159-160

SCHUSTER, M.F. 1979. Insect resistance in cotton Pages 101 -112 in Biology and breeding for resistance to arthropods and pathogens in agricultural plants, ed . M.K. Harris. Texas Agricultural Experiment Station, Coll e g e Station, Texas, USA.

SPARKS, A.N., CARPENTER, J.E., KLUN, J.A., and MULLINIX, B.G. 1979a. Field responses of male Helio• this zea (Boddie) to pheromonal stimuli and trap design. Journal of the Georgia Entomological Society 14:318 - 3 2 5

SPARKS, A.N., RAULSTON, J.R., LINGREN, P.D., CARPENTER, J.E., KLUN, J.A., and MULLINIX, B.G. 1979b. Field response of male Heliothis virescens to pheromonal stimuli and traps Bulletin of the Entomo l o g i • cal Society of America 25:268-274.

STIPANOVIC, R.D., BELL, A.A., O'BRIEN, D.H., and LUKEFAHR, M.J. 1977. Heliocide H2: an insecticidal sesterterpenoid from cotton (Gossypium). Tetrahedron Letter 6:567-570.

STIPANOVIC, R.D., BELL, A.A., O'BRIEN, D.H., and

LUKEFAHR, M.J. 1978a. Heliocide H1 : A n e w i n s e c t i c i • dal C25 terpenoid from cotton (Gossypium hirsutum). Journal of Agricultural and Food Chemistry 25:115-1 1 8 .

STIPANOVIC, R.D., BELL, A.A., O'BRIEN, D.H., and LUKEFAHR, M.J. 1978b. Heliocide H3, an insecticidal terpenoid from Gossypium hirsutum. Phytochemistry 17:151-152.

TINGLE, F.C., MITCHELL, E.R., and BAUMHOVER, A . H . 1978. Sex pheromone specificity in Heliothis. J o u r • nal of Chemical Ecology 4:471 -479.

2 3 9

The Chemist's Role in Host-Plant Resistance Studies

H. Rembold and E. Winter*

Abstract

Semiochemicals have been recognized as important factors in plant-insect interactions. Their terminology is explained. Recent work on crop-plant allomones is reviewed, with particular reference to their inhibitory effect on Heliothis adults or larvae. First data on the chemical composition of exudates collected from chickpea (Cicer a r i e t i n u m ; and pigeonpea (Cajanus cajan) varieties at ICRISAT are presented. In chickpea, the contents of malate—expressed as percentage of total dry matter-decrease with increasingly moist conditions, from 100 to less than 50%. Intervarietal differences in the capacity of malate excretion under stress conditions can be demonstrated. Heliothis damage is high with low malate concentration, and vice versa. A more complicated picture of repelling and attracting compounds is shown in the chemical analysis of pigeonpea exudates. Malate plays a minor role here, whereas various compounds not yet identified show intervarietal differences. Their occurrence and relative proportions under different environmental conditions are discussed. Finally, interaction of endogenous plant-specific factors and those originating from the environment and their involvement in host-plant x pest-insect interaction are described.

T h e p r o b l e m s of e n v i r o n m e n t a l hazards often enemies, autocidal techniques, and the integration associated with conventional broad-spectrum of c o m p l e m e n t a r y techniques s u c h as a gron omi c insecticides and of an increasing number of practices. However, many of these highly attractive insecticide-resistant pests are all too apparent. approaches have proceeded only slowly or even They have led to a search for more selective and failed to capitalize on new knowledge. There may biodegradable insecticides and to studies on host- be many reasons for this, s u c h as e c o n o m i c plant resistance, insect attractants, use of natural constraints—broad-spectrum insecticides can be manufactured in bulk and sold for use against a wide array of pests—or organizational factors. *Insect Biochemistry Group, Max-Planck-lnstitut fur Biochemie, Martinsried bei Munchen, Federal Republic of Germany. However, our greatest barrier against the practical

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management 15-20 November 1981, Patancheru, A.P., India 241 application of semiochemicals (from Greek (allelochemicals). In their comprehensive review of semeon, a mark or signal) in plant protection semiochemicals and their role in pest control, comes from our ignorance in this no-man's land Nordlund et al. (1981) tabulate the various kinds of between basic and applied biology. During a rela• chemical-releasing stimuli. Table 1 gives a shor• tively long period of complete reliance on conven• tened and simplified definition of this terminology. tional pesticides, the understanding of fundamental More familiar are the terms arrestant, attractant, processes involved in plant-insect interaction has repellent, stimulant, and deterrent. The combined not been appreciated by the scientist. The transla• use of both terminologies may be recommended, tion of biological principles into chemical signals as a kairomone emitted by species A causing reac• and their incorporation into applied programs tions in species B with beneficial results for B may therefore often fails in default of biological under• be an attractant, arrestant, or stimulant tor species standing on the chemist's as well as on the biolo• B. gist's side. We have yet to recognize that the concept of integrated pest management must incorporate new aspects derived from semio• chemicals. The real challenge of the future will be Chemistry of Plant-Insect the biochemical understanding of the selection Interaction pressure arising from crop monocultures, which finally establishes a few main pests resistant When investigating the significance of semio• against our traditional insecticide management. chemicals in insect-plant interactions, the chem• One of these pests may become Heliothis. ist's view is primarily directed to allelochemicals, The semiochemicals (Law and Regnier 1971) i.e., substances interspecific in nature. The other are subdivided into two major groups, depending group, the pheromones, has been proven as a on whether the interactions between organisms potential tool in insect pest management (insect- are intraspecific (pheromones) or interspecific trapping, c.f. Flint and van den Bosch 1981). How-

Table 1. Chemical-releasing stimuli.

Hormone: A chemical agent produced by a tissue or endocrine g land. Controls physiological processes within an organism.

Semiochemical: A chemical involved in the interaction between orga n i s m s .

1. Pheromone: A substance externally secreted by an organism caus ing a specific reaction in a receiving organism of the same s p e c i e s .

2. Allelochemical: A substance significant to an organism of a different species for reason other than food as such.

a. Allomone : A substance produced by an organism of species A. R e c e i v e d b y species B, it causes a reaction in B that is favora ble to A, not t o B.

b. Kairomone: Similar to allomone, but reaction in B is favorable t o B .

c. Synomone: Similar to allomone, but reaction in B is favorable to A and B.

d. Apneumone: A substance emitted by nonliving material, favorabl e t o s o m e species and detrimental to o t h e r s .

Source: Nordlund (1981).

2 4 2 ever, a m u c h m o r e diverse a n d exciting field has (cf. Norris and Kogan 1980). Whereas these com• become the study of insect-host-plant interactions. pounds have a detrimental effect on the insect's Schoonhoven (1981) summarizes the present growth, others interfere with its endocrine system knowledge of the role of chemical mediators ( p r e c o c e n e from Ageratum houstonianum, B o w e r s between plants and phytophagous insects in five et al. 1976; azadirachtin from Azadirachta indica, t h e o r e m s : Rembold and Sieber 1981). In spite of the vast array of allomones present in 1. All plants have allomones that protect them from the plant kingdom, there are insects that tolerate insects (and other organisms). allomones even in plants containing well-known 2. S o m e insect species tolerate the p r e s e n c e of broad-spectrum insecticides, such as Chrysanthe• allomones from certain plant species. mum, Derris, and Nicotiana. Only a few cases have 3. Some insect species exploit these substances been analyzed in sufficient detail to elucidate the a n d use t h e m as kairomones in the recognition of nature of tolerance. Many chemicals can be their host plants. broken down by mixed-function oxidases of the 4. Concomitant with behavioral preferences, physi• insect gut or fat-body (Krieger et al. 1971), or be ological adaptations are present, maximizing the eliminated by other physiological mechanisms insect's nutritional efficiency on specific food (review: Brattsten 1979). Here, plants and insects plants. wage a continual evolutionary battle, as Schoon• 5. Plant-insect relationships evolve continuously, hoven (1981) mentioned in his final theorem, a n d and an apparent status quo exists only at the chemists and plant breeders have to keep p a c e instant of our observation. with this evolution. In this paper we will give e x a m p l e s for these five In conclusion of this brief overview, we should theorems, concentrating on Heliothis or lepidopter- not overlook the fact that plants also emit kairo• ous species. The following work gives an insight mones beneficial to the insects, mainly in their into the chemical interaction of this insect with crop host-plant recognition. Lepidopterous larvae have plants. a very small number of chemoreceptors, but yield a Bottger et al. (1964) had already found a relation• highly detailed image of the plant's chemical con• ship between gossypol content of cotton plants and stitution (electrophysiological measurements, their insect resistance. Lukefahr and Martin (1966) Schoonhoven 1969). The recognition of sugars e x t e n d e d this work a n d incorporated the pigments a n d amino acids was investigated for larvae of of cotton into artificial diets for Heliothis zea a n d Heliothis zea by Dethier and K u c h (1971). H o w • Heliothis virescens larvae, of which less than 30% ever, some substances that seem to be allomones r e a c h e d the pupal stage w h e n the diet c o n t a i n e d may at the s a m e time have a kairomone effect, as 0.2% gossypol. Later, compounds other than gos• was demonstrated by an increased egg-laying of sypol (heliocides) were isolated from cotton and Heliothis armigera onto muslin cloth sprayed with s h o w n as toxic to Heliothis virescens. T h e s u b s t a n • malic acid from chickpea exudates compared with ces are terpenoids (Stipanovic et al. 1978) or tan• water-sprayed muslin (ICRISAT 1978/79). nins and phenols (Hedin et al. 1980). From corn In this complex and interwoven field of c h e m i c a l {Zea mays) a flavone-C-glycoside was isolated interaction between plants and insects, it is difficult a n d p r o v e n to inhibit growth a n d d e v e l o p m e n t of to determine the chemical basis of plant resistance Heliothis zea (Elliger et al. 1980), a n d in t o m a t o to herbivorous attacks. Comparatively increased leaves (Lycopersicon esculentum) the phenolic resistance of a certain plant species or variety is compounds (mainly flavonol glycosides like rutin) most certainly based on the special b a l a n c e of e x c r e t e d by the glandular t r i c h o m e s w e r e s h o w n to repelling and attracting semiochemicals, their con• contribute substantially to the growth-inhibiting centration in and on the aerial parts of the plant, the effect of these leaves on larvae of Heliothis zea capacity of the plant to produce or e x c r e t e these (Duffey a n d Isman 1981). chemicals, and the effect these c h e m i c a l s have on Further plant allomones under investigation are the key insect pest. Other factors may be of equal the trypsin inhibitors in legume seeds (e.g., in importance, s u c h as the life c y c l e of the plant a n d c h i c k p e a , Cicer arietinum, Belew et al. 1975) that insect, insect population density during the life disturb the insect's digestion, and other allomones cycle of the plant, morphological defense mecha• such as acetogenins, alkaloids, and aromatics, nisms in the plant, nutritional status of the plant, a n d w h i c h are derived f r o m shikimic a c i d a n d a c e t a t e susceptibility to environmental changes.

2 4 3 The Concept of Concerted segregated breeding material will follow. Interaction In principle, our chemical approach to the field of plant-insect relationship differs from those

From observation through many years, a series of reviewed at the beginning of this paper. We use the chickpea (Cicer arietinum) and pigeonpea (Caja- concept of a concerted interaction of allelochemi- nus cajan) varieties has been selected at ICRISAT cals, which may be attractants and repellents for with a comparatively low susceptibility to Heliothis the larva, oviposition stimulants and deterrents for attack. These pedigrees offer a promising collec• the adult female, or growth inhibitors for different tion of semiochemicals for the analytical chemist. If developmental stages of certain pests. Only the should be possible to help the breeder in segregat• orchestration of these many chemical signals indu• ing new resistant varieties by following the pres• ces the response on the insect's side. ence of chemical signals quantitatively. These data can be collected in the glasshouse and then com• pared with field data. On this basis, we started a Malate Excretion and Heliothis collaborative project with ICRISAT Pulse Entomol• Damage in Chickpea ogy and the Max-Planck Institute (MPI), beginning about 1 year ago and financed by Deutsche Both Cicer arietinum a n d Cajanus cajan have Gesellschaft fur Technische Zusammenarbeit. glands on their whole surface. In chickpea, these This 2-year project has aimed at selection of 10 to glands excrete large amounts of a fluid, visible as 20 varieties with low, moderate, and high borer droplets all over the plant. Exudation depends on damage. These varieties are grown under three temperature and growth stage and increases environmental situations: (1) on dry soil at ICRISAT, towards the reproductive stage (Koundal and (2) on humid soil at ICRISAT, and (3) on humid soil Sinha 1981). The exudate can easily be collected in a glasshouse at MPI, Martinsried. Comparative with cotton plugs in amounts of milliliters, and we analysis is made by GC, GC-MS, and HPLC primar• have used this method for a first screening of 12 ily of their respective exudates. chickpea varieties that were either grown on dry The philosophy behind this initial program is to soil or on a spot near Lake ICRISAT (Table 2). All collect information on the following questions: the samples were extremely acidic, with pH value close to 1.2, which explains the well-known repel• 1. Are there prominent compounds present in the ling effect of the exudate. The malic acid (malate), exudate that can be correlated with pod damage, contained in concentrations of 10 to 56%, is seasonal differences between flowering and insect responsible for the low pH, and the susceptibility to population, soil quality, humidity, and photo• Heliothis attack follows these concentrations synthesis? (Rembold 1981) In other words, borer damage was 2. How does each of these varieties respond to found low in chickpea varieties that excrete highly stress situations? Is there a collapse in resistance concentrated malic acid. factors? Are some of them more resistant than Are there any other compounds contained in the others? These data could help us to better under• exudates of the 12 chickpea varieties mentioned? stand the breakdown of some highly resistant var• Figure 1 gives the malate amounts contained in the ieties when transferred to other continents or even dry matter. There are, of course, intervarietal differ• to other nearer locations. ences; malate is the main component, with about 3. How stable are the chemical characteristics in 70 to 100% and there may be other compounds successive years, and eventually, under different present, which may also function as allelochemi- conditions of climate, insect population density, cals. However, carefully collected data on pod flowering season, etc.? d a m a g e a n d Heliothis population in the test plots After a period of 2 years, it should be clear are still lacking. whether such a chemical approach can add impor• These preliminary data already demonstrate that tant information to the understanding of host-plant in exudates collected in the field near the lake, the resistance to insect pests. If these questions can proportion of malate in the dry matter was generally be positively answered—and the data from our first lower, a n d Heliothis damage was always higher year's work already indicate that they can—then a than in the same cultivars on dry soil. These analyt• second 3-year period of extensive biochemical, ical data demonstrate a sensitive reaction of the entomological, and fiela studies with carefully chickpea's metabolism to its environment. This

2 4 4 T a b l e 2 . B o r e r d a m a g e (%) i n c h i c k p e a s a m p l e s c o l l e c t e d from unsprayed plots: location 1 (BA27) and location 1 1 (BA24A) at ICRISAT farm, poatralny season, 1980-81.

L o c a t i o n 1 B A 2 7 ( d r y ) L o c a t i o n I I B A 2 4 ( A ) ( W e t )

S a m p l e D a y s t o 5 0 % M e a n p o d D a y s t o 5 0 % M e a n p o d N o . P e d i g r e e f l o w e r i n g d a m a g e f l o w e r i n g d a m a g e (%) (%)

1 I C C - 5 0 6 5 4 2 . 0 4 9 5 . 5 2 8 5 0 - 3 / 2 7 7 9 8 . 1 NA 3 A n n i g e r i - 1 5 8 6 . 3 4 9 2 2 . 6 4 C - 2 3 5 9 6 7 . 6 7 7 1 3 . 0 5 G - 1 3 0 NA 8 4 2 1 . 7 6 I C C - 5 7 1 6 5 6 4 . 8 NA 7 I C C - 3 9 9 9 9 3 4 . 6 7 4 1 1 . 9 8 J G - 7 4 5 8 9 . 1 NA 9 I C C - 5 2 6 4 1 0 3 6 . 4 7 7 1 9 . 6 1 0 L - 5 5 0 8 6 1 4 . 4 6 3 1 8 . 6 11 I C C L - 7 8 0 0 9 NA 6 3 1 8 . 0 1 2 I C C - 1 0 6 1 9 NA 5 6 4 . 8

becomes dramatically evident if exudates are ana• by M. obtusa and mainly occurs in the early or lyzed from the same varieties grown in our glass- mid-flowering cultivars, abating in the late- house at Martinsried: malate content in the dry flowering ones, when M. obtusa starts its attack. matter is generally reduced. However, some of the The cultivars were ordered according to their flow• varieties are more stable in their malate excretion ering times to show a possible interrelation of dam • under these conditions than others. The exudates age rates with insect population densities (data we in the dry matter also contain a series of other still have to add to this scheme). Low Heliothis compounds, some of which may act as attractants damage in late-flowering cultivars may be due to a and so explain the breakdown of resistance under low insect population, but within the mid-flowering changing environmental conditions (Rembold cultivars there are some outstandingly susceptible 1980). Interestingly enough, in the glasshouse ones (7 and 14). Gas chromatography of silylated experiment, the exudates show the same intervar- dried samples of pod washings showed that either ietal differences as under moist conditions at ICRI- an extremely high content of total sugars in combi• SAT. This fact points to a variation of the genetic nation with a moderate amount of an unidentified capability amongst cultivars to produce malate, substance with a retention time of 434 seconds which needs to be studied in more detail. (cultivar 14), or low sugar contents with very low amounts of the unidentified substance (cultivar 7), are associated with highly damaged pods. Sugars Composition of Exudates vs and other substances seem to counteract by Heliothis Resistance in Pigeonpea attracting, and repelling, respectively, the insect. Malate seems to play a subordinate role in pigeonpea exudates, as its concentration is rather low. In contrast to chickpea, the surface in pigeonpea is Not all chemical components can be volatilized velvety, but without visible droplets. We therefore for GC analysis; therefore, HPLC was additionally collected the exudate by washing the pods with used. One peak of the diverse chromatograms (Fig. methanol. 3) showed obvious intervarietal differences (Fig. 2, In pigeonpea, two main insect pests endanger peak eluting after 474 sec.) that are similar to those yields: Heliothis armigera a n d Melanagromyza of the substance detected by GC analysis. HPLC- obtusa. Figure 2 shows that the pod damage isolation and silylation with subsequent GC analy- c a u s e d by H. armigera is higher than that caused

2 4 5 M a l a t e ( m g / m g dry 1.0 e x u d a t e )

0 . 8 p l a n t s from BA 27 ( dry)

p l a n t s from BA 2 4 A ( w e t ) 0 . 6

p l a n t s from M P J g l a s s - h o u s e (wet) 0 . 4

0 . 2

M e a n pod d a m a g e (%) 20 by H. armigera

On BA 27 (dry)

On BA 2 4 A ( w e t ) 0 D a y s to 5 0 % BA 2 4 A (wet) 49 - 49 - - 56 6 3 6 3 7 4 7 7 8 4 7 7 f l o w e r i n g BA 27 (dry) 54 56 58 58 7 9 - - 8 6 9 3 9 6 - 103

Cultivar No. 1 6 3 8 2 12 11 10 7 4 5 9

Figure 1. Pod damage and malate contents in the dry exudate of 12 chickpea cultivars (Cicer a r i e t i n u m ) listed according to days to 50% flowering. Malate contents of the exudates from plants grown at a dry location on ICRISAT fields under wet soil conditions there (Δ), and from a glasshouse experiment at the Max-Planck Institute, Germany (o). Malate was measured as TMS- derivative by glass capillary (SE 30) G C (Carlo Erba Fractovap with FID) and quantified by means of an integrator (Spectraphysics). For more details see Table 2.

sis showed that the two substances show similar experiment at MPI and is currently being examined intervarietal differences but are not identical. So far, from wet and dry fields at ICRISAT. t w o repellent s u b s t a n c e s have b e e n pointed out but not yet chemically identified or checked for their function as isolated substances in a bio-test. Conclusions The influence of environmental conditions on the quantity and chemical composition of the pigeon- The basic concept of plant-insect interaction p e a e x u d a t e s is being investigated in a g l a s s h o u s e t h r o u g h a c h e m i c a l signal has b e c o m e m o r e a n d

2 4 6 HPLC p e a k a r e a 5 0 (million counts)

peak 474 (sec)

4 4 0 5 2 0 . 9 1 . 2 1 . 6 0 . 4 0.6. 1.5 1.5 0.8 2.5 0.7 1.0 0.9

GC p e a k a r e a 1 0 0 (million counts)

5 0

G C - p e a k 4 3 4 ( s e c )

t o t a l

s u g a r s

m a l a t e

mean pod damage (%) by Melana- 2 5 - gromyza obtusa

Mean pod damage (%) b y 5 0 Heliothis armigera

days to 50% f l o w e r i n g 9 6 9 9 1 0 5 107 108 108 109 112 120 122 124 128 136 145 158

cultivar No. 1 2 3 9 8 6 12 7 14 4 5 15 11 10 13

Figure 2. Pod damage and occurrence of various substances in the pod exudates of 15 pigeonpea cultivars 9 Cajanus cajan) listed according to days to 50% flowering. For GC, the TMS-derivatives were used. For technical details compare Figure 1; cultivars are listed In Table 3.

2 4 7 T a b l e 3 . P e r c e n t a g e p o d d a m a g e I n p i g e o n p e a p o d s a m p l e s collected from unsprayed block (BA25) at ICRISAT farm, rainy season 1980-81.

S a m p l e D a y s t o 5 0 % P o d d a m a g e m e a n (%)

N o . P e d i g r e e f l o w e r i n g B o r e r P o d f l y T o t a l

1 P P E - 4 5 - E 2 9 6 1 8 . 1 2 . 3 2 3 . 9 2 I C P 7 2 0 3 - E 1 9 9 2 8 . 2 1 . 2 2 9 . 7 3 7 3 4 9 - 1 - S 4 1 0 5 2 8 . 2 2 . 5 3 1 . 2 4 7 9 4 6 - E 1 1 2 2 3 2 . 9 5 . 7 3 9 . 1 5 3 6 1 5 - E 1 1 2 4 3 0 . 4 1 7 . 4 4 9 . 3 6 1 6 9 1 - E 1 1 0 8 4 0 . 1 3 . 3 4 5 . 3 7 7 0 5 0 - E B 1 1 2 9 3 . 8 0 . 7 9 5 . 0 8 C - 1 1 1 0 8 4 3 . 9 3 . 5 5 1 . 7 9 lntg-1914-E2 1 0 7 2 5 . 2 1 . 9 2 7 . 5 1 0 ICP-7176-18-E2 1 4 5 1 3 . 0 2 3 . 0 4 5 . 7 1 1 8 1 3 4 - 1 -S1 1 3 6 1 1 . 2 1 6 . 1 3 7 . 2 1 2 8 1 0 - E 1 1 0 9 3 2 . 5 9 . 9 4 3 . 9 1 3 6 4 4 3 - E B 1 5 8 1 1 . 0 2 0 . 4 5 0 . 4 1 4 6 9 1 5 - E B 1 2 0 7 6 . 2 2 0 . 2 9 8 . 2 1 5 7 3 3 7 - 2 - S 4 1 2 8 1 8 . 1 3 9 . 4 7 6 . 1 1 6 Atylosia scarabaeoides 2 . 5 0 . 0 3 . 4 1 7 Atylosia sericea 1.1 0 . 0 1.1

more complicated with the detection of a multiplic• dominant malic acid. Quite another principle is ity of compounds with agonistic or antagonistic being used by pigeonpea. Here the concept of a effects on the pest insect. As plant protection prim• concerted action of semiochemicals is extensively arily means dealing with monocultures, one can, at used. If compared with pod damage, some com• least in principle, understand the immense selec• pounds are active as allelochemicals, others are tion pressure acting on the insect populations. If we inactive. It is obvious from these data that our basic want to protect our crops by methods other than approach of an analytical screening for marker toxic chemicals, we need a great deal of informa• compounds of varieties with different susceptibility tion about the host's and the insect's biochemistry, has been successful already and will have to be which is not available at present. The concept of e x t e n d e d in the future. However, it is most impor• semiochemicals will hopefully attract more scient• tant now to correlate these biochemical markers ists back to the no-man's land of new approaches and their quantity with insect behavior and crop- to pest control. plant metabolism under different environmental This integration of basic research with agricultu• conditions. From such studies we will get more ral problems of crop protection has been started in information about the extremely complicated our collaborative project with ICRISAT, and first- orchestration of the genetic, physiological, physi• still preliminary—data have been given, which may cal, and chemical factors that continuously influ• be summarized as follows. The two pulses under ence the insect pest as well as its host. Only such investigation obviously use two different methods an interdisciplinary endeavor will promote the con• for their protection. In chickpea, the excretion of a cept of integrated pest management. highly acidic compound in sometimes remarkably high concentrations of more than 50% of the exu• date, repels almost every insect. However, Helio- Acknowledgments this sometimes feeds even on this ideally protected plant. Future studies will have to clarify the pres• We are very grateful to Dr. W. Reed, Principal Ento- ence of other semiochemicals besides the pre• mologist, a n d Dr. S.S. Lateef, Entomologist, at ICRI-

2 4 8 SAT for their continuous help and interest. Skilful technical assistance by Mrs. Grune is gratefully acknowledged. Our own project is supported by GTZ, Eschborn, contract No. 72.7866.6-26.300. 4 7 4 s e c

References

BELEW, M., PORATH, J., and SUNDBERT, J. 1975. T h e trypsin a n d c h y m o t r y p s i n inhibitors i n c h i c k p e a s ( C i c e r arietinum L.). European Journal of Biochem• istry 60: 2 4 7 - 2 5 8 .

BOTTGER, G.T., SHEEHAN, E.T., and LUKEFAHR, M . J . 1964. Relation of gossypol content of cotton plants to insect resistance. Journal of Economic Entomology 57(2):283-85.

BOWERS, W.S., OHTA, T., CLEERE, J.S., and MAR- SELLA, P.A. 1976. Discovery of insect anti-juvenile hor• m o n e s in plants. S c i e n c e 193: 5 4 2 - 5 4 7 .

BRATTSTEN, L.B. 1979. Biochemical defense mecha• nisms in herbivores against plant allelochemics. Pages 1 9 0 - 2 7 0 in Herbivores: their interaction with secondary plant metabolites, eds. G.A. Rosenthal and D.H. Janz e n . New York, USA: Academic Press.

DETHIER. V.G., and KUCH, J.H. 1971. Electrophysio• logical studies of gustation in lepidopterous larvae. I. C o m p a r a t i v e sensitivity t o sugars, a m i n o a c i d s a n d g l y c o - sides. Zeitschrift fur vergleich ende Physiologie 72: 3 4 3 - 3 6 3 .

DUFFEY, S.S., and ISMAN, M.B. 1981. Inhibition o f insect larval growth by phenolics in glandular trichome s of tomato leaves. Experientia 37: 574-576.

ELLIGER, C.A., CHAN, B.G., WAISS, A.C., Jr., LUDIN, R.E., and HADDON, W.F. 1980. C - glycosylflavones from lea mays that inhibit insect devel• opment. Phytochemistry 19: 293-297.

FLINT, M.L., and VAN DEN BOSCH, R. 1981. Intro• duction to integrated pest management. New York, USA: P l e n u m Press.

HEDIN, P.A., COLLUM, D.H., WHITE, W.H., PAR- 0 10 m i n ROTT, W.L., LANE, H.C., and JENKINS, J.N. 1980. T h e c h e m i c a l basis for r e s i s t a n c e in c o t t o n to Heli- othis insects. P a g e s 1071 - 1 0 8 6 in Scientific P a p e r s of t h e Figure 3. Characteristic HPLC chromatogram Institute of Organic and Physical Chemistry of Wroclaw of the methanoiic pod washings of C a j a n u s Technical University No.22, eds. F. Sehnal, A. Zabza, J.J. Menn and B. Cymborrowsky. Wroclaw Technical Univer- c a j a n plants from ICRISAT field trials. The sity Press, Wroclaw, Poland. arrow points to the peak at 474 sec, the s u b - stance expressed in Figure 2, upper part, for all ICRISAT. 1979. Pulse E n t o m o l o g y ( c h i c k p e a ) D e p a r t • varieties. For HPLC Pye Unicam equipment (PU mental Progress Report-4, Patancheru, A.P., India. 4010 Pump, LC-UV-Detector, PM 8252 Mimeographed.

Recorder) was used. Analytical wavelength 215 KOUNDAL, K.K., and SINHA, S.K. 1981. M a l i c a c i d nm. Column: ODS Hypersil (5 µ), 250 x 5 mm. e x u d a t i o n a n d p h o t o s y n t h e t i c c h a r a c t e r i s t i c s in Cicer Eluent: 6 5 % methanol in water. arietinum. Phytochemistry 20(6):1251-1252.

2 4 9 K R I E G E R , R.I., F E E N Y , P.P., a n d W I L K I N S O N , C . F . 1 9 7 1 . D e t o x i c a t i o n e n z y m e s i n t h e g u t s o f caterpillars: a n evolutionary a n s w e r t o plant d e f e n s e s ? S c i e n c e 1 7 2 : 5 7 9 - 5 8 1 .

L A W , J . H . , a n d R E G N I E R , F.E. 1 9 7 1 . Pheromones. Annual Review of Biochemistry 40: 533-548.

L U K E F A H R , M . J . , and M A R T I N , D . F . 1 9 6 6 . C o t t o n - plant p i g m e n t s as a s o u r c e of r e s i s t a n c e to the b o l l w o r m and tobacco budworm. Journal of Economic Entomology 59(1):176-179.

N O R D L U N D , D.A., J O N E S , R . L . , a n d L E W I S , W . J . (eds.) 1 9 8 1 . S e m i o c h e m i c a l s : their role in pes t c o n t r o l . N e w Y o r k , U S A : Wiley.

N O R D L U N D , D.A. 1 9 8 1 . S e m i o c h e m i c a l s : a r e v i e w o f the terminology. P a g e s 1 3 - 2 8 in Semiochemicals, their role in pes t c o n t r o l , e d s . D.A. N o r d l u n d , R.L. J o n e s , a n d W.J. L e w i s . N e w York, USA: Wiley.

N O R R I S , D . M . , and K O G A N , M . 1 9 8 0 . Biochemical and morphological bases of resistance. Pages 23-61 in B r e e d i n g p l a n t s resistant t o i n s e c t s , e d s . F.G. M a x w e l l a n d P R . J e n n i n g s . N e w Y o r k , U S A : Wiley.

R E M B O L D , H . 1980. Chemical aspects of plant resist• a n c e against insects. T r a n s a c t i o n s B o s e R e s e a r c h Insti• t u t e 4 3 : 5 3 - 6 3 .

R E M B O L D , H . 1 9 8 1 . M a l i c a c i d i n c h i c k p e a e x u d a t e — a m a r k e r for Heliothis resistance. International Chickpea N e w s l e t t e r 4 : 1 8 - 1 9 .

R E M B O L D , H . , and S I E B E R , K.P. 1 9 8 1 . Inhibition o f oogenesis and ovarian ecdysteroid synthesis by azadi- rachti n in Locusta migratoria migralorioides (R.+ F ) . Zeitschrift fur N a t u r f o r s c h u n g 3 6 : 4 6 6 - 4 6 9 .

S C H O O N H O V E N , L . M . 1969. G u s t a t i o n a n d f o o d - p l a n t selection in some, lepidopterous larvae. Entomologia E x p e r i m e n t a l i s e t A p p l i c a t a 12: 5 5 5 - 5 6 4 .

S C H O O N H O V E N , L . M . 1 9 8 1 . Chemical mediators between plants and phytophagous insects. Pages 31 -50 in S e m i o c h e m i c a l s , their role in pest c o n t r o l , e d s . D.A. N o r d l u n d , R.L. J o n e s , a n d W . J . L e w i s . N e w York, USA: Wiley.

S T I P A N O V I C , R . D . , B E L L , A . A . , O ' B R I E N , D . H . , a n d L U K E F A H R , M . J . 1 9 7 8 . Heliocide H; A new insecticidal C25 t e r p e n o i d f r o m c o t t o n ( G o s s y p i u m hirsutum). J o u r n a l of Agricultural and Food Chemistry 26(1):115-118.

2 5 0 Progress in Research on Chemical Aspects of Host-Plant Resistance to Heliothis zea in Corn, Soybean, and Tomato

A.C. Waiss, Jr., R.G. Binder, B.G. Chan, C.A. Elliger and D.L. Dreyer*

Abstract

Inhibitors of Heliothis zea larval growth have been isolated from corn, soybean, and tomato plants, and have been identified. Isolation procedures, biological activities, and significance of these compounds in plant resistance to H. zea are discussed.

For several years, our research group in California ate separately or possibly synergistically. has tried to determine phytochemical bases tor the The presence in corn silk of a factor lethal to cor n resistance to insect pests shown by some eco• earworm larvae was reported by Walter (1957) and nomically important host plants. We hope to confirmed by Wann and Hills (1966). However, no become able to use specific analyses of plant work relating chemical composition of corn silk to chemicals to recognize plants that have good likeli• biological activity was reported until recently, hood of showing resistance and thereby help plant when—with the cooperation of scientists at the breeders and entomologists select more efficiently Small Grain Insect Laboratory, Tifton, Georgia, and for insect-resistant plant varieties. the University of Missouri, Columbia, Missouri—we This paper reports some of the work done and isolated a novel compound from the methanolic progress made in isolating and identifying growth extract of silk of a resistant line (var. Zapalote inhibitors of Heliothis zea larvae from corn, soy• Chico), chemically characterized this compound, bean, and tomato and to discuss the roles of these maysin, and showed that it was an effective larval compounds in plant protection. I shall omit our growth inhibitor for H. zea (Waiss et al. 1979). contributions to the understanding of cotton-H. zea Growth of corn earworm larvae fed 0.15% (w/w) interactions because this work is well documented maysin in a synthetic diet for 12 days was only 50% elsewhere (Chan et al. 1978a, 1978b; Elliger et al. as much as for larvae fed control diet. In addition to 1978; Waiss et al. 1981a, 1981b). maysin, the 3'-methyl ether and 3'-de-oxy deriva• tives of maysin were also isolated from Zapalote Chico silk (Elliger et al. 1980a). These compounds H. zea Larval Growth Inhibitors occur at lower concentrations than maysin and are in Corn less active against H. zea. Maysin has an absorption maximum at 352 nm in The resistance of certain corn varieties to attack by the ultraviolet spectrum. Therefore, comparison of corn earworm has been ascribed both to chemical relative absorptivities of corn-silk extracts at this and morphological factors. These factors, with per• wavelength has been used as a measure of relative haps varying degrees of effectiveness, might oper- and maximum maysin content in corn silk. In 1980, nine corn genotypes planted at five locations (Tifton, Georgia; Geneva, New York; *U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Berkeley, California, USA. Columbia, Missouri; Union City, Tennessee; and

International Crops Research Institute for the Semi- Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India 251 Oahu, Hawaii) were evaluated for relative maysin nitrogen, carbohydrates, organic acids, and sterols content of their silk. Initial results indicate that there (Tester 1977). The resistant cultivars had lower is little correlation between the amount of maysin in nitrogen content, a larger amount of soluble carbo- the silk and the location of the planting, regardless hydrates, and at flowering and pod-filling, a greater of differences in climate and daylength. What may amount of sterols. Recently, Grunwald and Kogan be especially interesting and important is that may- (1981) determined the sterol composition of insect- sin content varies greatly (up to 20-fold) within a susceptible and -resistant soybean varieties and corn line and that crosses between corn varieties lines and concluded that resistance to insect produce F1 offspring with higher maysin levels in attack is not due to a sterol imbalance or unusual their silk than is found in the silk of either parent. We sterol makeup of the soybean leaf. Analyses of therefore hope that the use of a recurrent selection benzoic and cinnamic acid derivatives from injured technique in breeding could be used to increase and noninjured leaves of a resistant and a suscept• maysin content and thereby increase resistance to ible cultivar (Hardin 1979) showed differences in corn earworm. amounts from these tissues. However, even the Data from the interregional experiment also indi• highest concentration found seems, based on our cate that the amount of maysin in corn silk dimin• bioassays with these compounds (Chan, unpub• ishes as much as 80% in the 20 days after anthesis lished), to be too low to be effective in antibiosis to (pollination). We hypothesize that changes in the H. zea. silk after pollination allow reaction of polyphenol To bioassay soybean phytochemicals, we incor• oxidase with the polyphenolic maysin to give poly• porate leaf extracts or fractions thereof in an artifi• meric compounds. These polymeric compounds, cial diet for the bollworm (Chan et al. 1978c). When similar to condensed tannin (Chan et al. 1978b), extracts of dry leaves are obtained by successive also inhibit growth of corn earworm larvae; thus extraction with heptane, ethyl acetate, acetone, simply determining maysin content would not give methanol, and water and put into the bollworm diet an adequate estimation of the antibiotic potential of in amounts essentially equivalent to amounts the corn silk. Currently, efforts in our laboratory are obtainable from fresh leaves, larvae fed a diet con• directed toward developing an improved analysis taining the heptane, ethyl acetate, or acetone for total phenolic compounds in corn silk. Subse• extracts weigh modestly more at 12 days old than quently, observations of corn-earworm damage do control larvae. However, they weigh substan• will be compared with content of phenolic com• tially less when fed diet containing the methanol or pounds in the silk. water extracts, being generally 40 to 75% the size of control larvae. If fed combined methanol and water extracts, larvae at 12 days are about one- Antibiotic Constituents of Soybean third the size of control larvae. From the methanol extract, we have isolated a In a comparison of experimental and commercial compound that seems to be largely responsible for cultivars of soybean, Clark et al. (1972) found sev• the weight-gain reduction activity of this extract. eral cultivars that exhibited significantly greater This compound is pinitol, a monomethyl ether of resistance to the bollworm than did the commercial chiro-inositol, also found in soybean leaves in cultivars. Among larvae fed on the plant introduc• smaller amounts. With 0.7% pinitol in their diet, tions, mortality was higher, weight gains were 12-day-old larvae were 50% the size of control reduced, and time to pupation was longer than in larvae (Dreyer et al. 1979). W h a t is the role of pinitol larvae fed on commercial cultivars (Hatchett et al. in soybean host-plant resistance? This is difficult to 1976). In larvae fed PI-229358 leaves, mortality answer. Content of pinitol in soybean leaves is occurred predominantly in the later instars and variable, depending on cultivar, stage of develop• appeared to be due to difficulties in molting (Bela n d ment, a g e of leaf on the plant, a n d e v e n time of day and Hatchett 1976). Differences in mortality were (Dougherty 1976; Binder unpublished). Indeed, attributed to differences in the age of leaves fed pinitol has been identified as a feeding stimulant for and to stage of plant growth (Beland and Hatchett another lepidopteran, the yellow butterfly (Numata 1976; McWilliams and Beland 1977). et al. 1978)! In one study, two insect-resistant and two sus• We are trying to identify compounds in the water ceptible soybean cultivars were analyzed at differ• extract that restrict larval growth but do not have a ent growth stages for their contents of total specific identification yet.

252 Feeding larvae the methanol and water extracts CHAN, B.G., WAISS, A.C., Jr., BINDER, R.G., and lengthens the time to pupation, but the majority do ELLIGER, C.A. 1978a. Inhibition of Lepidopterous larval successfully pupate and emerge. An interestingly growth by cotton contituents. Entomologia Experimental i s different situation prevailed for larvae fed the hep• et Appllcata 24:94-100.

tane extract of PI-229358 soybean leaves. CHAN, B.G., WAISS, A.C., Jr., and LUKEFAHR, M.J. Throughout their development they were as large 1978b. Condensed tannin, an antibiotic chemical from as controls or larger, yet the majority was unable to G o s s y p i u m hirsutum. Journal of Insect Physiology pupate successfully. Mean day of death was 20.8, 24:113-118.

whereas mean day of pupation was 17.3 for control CHAN, B.G., WAISS, A C , Jr., STANLEY, W.L., and larvae. Overall mortality was about 85%. Larvae fed GOODBAN, A.E. 1978c. A rapid diet p r e p a r a t i o n a combination of all extracts experience both method for antibiotic phytochemical bioassay. Journa l of delayed pupation and high mortality. Economic Entomology 71:366-368.

Clearly, feeding of leaf extracts evinces much of CLARK, W.J., HARRIS, F.A., MAXWELL, F.S., and the antibiotic activity that is given by feeding of HARTWIG, E.E. 1972. R e s i s t a n c e o f c e r t a i n s o y b e a n leaves and thus offers us encouragement in our cultivars to bean leaf beetle, striped blister beetle a n d search for phytochemicals responsible tor host- bollworm. Journal of Economic Entomology 65:1669- plant resistance. 1 6 7 2 .

COSENZA, G.W., and GREEN, H.B. 1979. Behavior of the t o m a t o f r u i t w o r m , Heliothis zea (Boddie), on suscepti• H. zea Larval Growth Inhibitors ble and resistant lines of processing tomatoes. Hortic u l t u • in Tomato ral Science 14:171-173.

DOUGHERTY, D.E. 1976. Pinitol and other soluble car• The presence of chemical factors in tomato leaves bohydrates in soybean as factors in facultative parasite antibiotic to H. zea was reported by Fery and Cuth- nutrition. Ph.D. thesis, University of Georgia, Ga, USA. bert in 1975. Later, Cosenza and Green (1979) DREYER, D.L., BINDER, R.G., CHAN, B.G., WAISS, gave evidence for both nonpreference and antibio• A.C., Jr., HARTWIG, E.E., and BELAND, G.L. sis to account for reduced damage in certain 1979. Pinitol, a larval growth inhibitor for Heliothis zea in tomato lines. Recently, Williams et al. (1980) disco• soybean. Experientia 35:1182-1183. vered 2-tridecanone in the wild tomato Lycoper- sicon hirsutum f. glabratum, d e s c r i b e d it as a DUFFEY, S.S., and ISMAN, M.B. 1981. Inhibition o f insect larval growth by phenolics in glandular tricho m e s natural pesticide, and suggested improving the of tomato leaves. Experientia 37-574-576. insect resistance of domestic tomatoes by breed• ing with the wild variety. ELLIGER, C.A., CHAN, B.G., and WAISS, A.C. Jr., In our laboratory, we found that not one com• 1978. Relative toxicity of minor cotton terpenoids com• pared to gossypol. Journal of Economic Entomology pound but rather a group of diverse compounds is 71:161-164. responsible for the reduction of H. zea d a m a g e to tomato plants (Elliger et al. 1981). These com• ELLIGER, C.A., CHAN, B.G., WAISS, A.C. Jr., LUN- pounds are tomatine, a glycoalkaloid that is feeding DIN, R.E., and HADDON, W.F. 1980a. C - deterrent to the potato beetle and other insect Glycoflavones from Zea mays that inhibit insect development. Phytochemistry 19:293-297. pests of potato; rutin; chlorogenic acid; and caffeyl esters of glucaric acid. The effectiveness of rutin in ELLIGER, C.A., CHAN, B.G., and WAISS, A.C. Jr., retarding the growth of Heliothis species has been 1980b. Flavonoids as larval growth inhibitors: structural reported (Lukefahr and Martin 1966; Chan et al. factors governing toxicity. Naturwissenschaften 67:33 8 - 1978a) and the presence of rutin in the glandular 3 3 9 . trichomes of tomato plants has been suggested as ELLIGER, C.A., WONG, Y., CHAN, B.G., and WAISS, a factor in the inhibition of larval growth on tomat o A.C., Jr., 1981. G r o w t h inhibitors i n t o m a t o (Lycoper- plants (Duffey and Isman 1981). sicon) to t o m a t o fruitworm {Heliothis zea ). Journal of Environmental Ecology (in press).

FERY, R.L., and CUTHBERT, F.P. 1975. Antibiosis in Lycopersicon to t o m a t o f r u i t w o r m (Heliothis zea). J o u r n a l References of the American Society of Horticulture 100:276-278.

BELAND, G.L., and HATCHETT, J.H. 1976. E x p r e s • GRUNWALD, C., and KOGAN, M. 1981. Sterols of soy• sion o f antibiosis t o t h e b o l l w o r m i n t w o s o y b e a n g e n o • beans differing in insect resistance and maturity group . types. Journal of Economic Entomology 69:557-560. Phytochemistry 20:765-768.

2 5 3 HARDIN, J.M.T. 1979. Phenolic acids of soybeans res• istant and nonresistant to leaf feeding larvae. M.S. thesis, University of Arkansas, Fayetteville, Ark, USA.

HATCHETT, J.H., BELAND, G.L., and HARTWIG, E.E. 1 9 7 6 . Leaf-feeding resistance to bollworm and tobacco budworm in three soybean plant introductions . Crop Science 16.277-280.

LUKEFAHR, M.J., and MARTIN, D.F. 1966. C o t t o n plant pigments as a source of resistance to the bol l w o r m and tobacco budworm. Journal of Economic Entomology 59:176-179.

McWILLIAMS, J.M., and BELAND, G.L. 1977. Boll- worm: effect of soybean leaf age and pod maturity o n development in the laboratory. Annals of the Entomo l o g i • cal Society of America 70:214-216.

NUMATA, A., HOKIMOTO, K., SHIMADA, A., YAMA- GUCHI, H., and TAKAISHI, K. 1978. Feeding stimu• lants for the larvae of the yellow butterfly, Eurema hecabe mandarina (Lepidoptera: Pieridae). Applied Entomology and Zoology 13(2):133-135.

TESTER, C.T. 1977. Constituents of soybean cultivars differing in insect resistance. Phytochemistry 16:1 8 9 9 - 1 9 0 1 .

WAISS, A.C., Jr., CHAN, B.G., ELLIGER, C.A., WISE- MAN, B.R., McMILLIAN, W.W., WIDSTROM, N.W., ZUBER, M.S., and KEASTER, A.J. 1979. Maysin, a flavone glycoside from corn silks with antibiotic activity. Journal of Economic Entomology 72:256-258.

WAISS, A.C., Jr., CHAN, B.G., ELLIGER, C.A., and BINDER, R.G. 1981a. Biological active cotton constitu• ents and their significance in HPR. Pages 61 -63 in P r o • ceedings, Beltwide Cotton Improvement Research Conference, 5-10 Jan 1981, New Orleans, La, USA.

WAISS, A.C., Jr., CHAN, B.G., ELLIGER, C.A., DREYER, D.L., BINDER, R.G., and GUELDNER, R.C. 1981b. Insect growth inhibitors in crop plants. Bulletin of the Entomological Society of America. (In press.)

WALTER, E.V. 1957. Corn earworm lethal factor in silk of sweet corn. Journal of Economic Entomology 50:10 5 - 1 0 6 .

WANN, E.V., and HILLS, W.A. 1966. E a r w o r m resist• ance in sweet corn at two stages of ear development . American Society of Horticultural Science 89: 491 - 4 9 6 .

WILLIAMS, W.G., KENNEDY, G.G., YAMAMOTO, R.T., THACKER, J.D., and BORDNER, J. 1980. 2 - Tridecanone: A naturally occurring insecticide from t h e wild tomato Lycopersicon hirsutum f. glabratum. S c i e n c e 207:888-889.

2 5 4 Techniques for Efficient Mass Rearing and Infestation in Screening for Host-Plant Resistance to Corn Earworm, Heliothis zea

John A. Mihm*

Abstract

This paper presents the experience accumulated and techniques developed at CIMMYT (Centro Internacional de Mejoramiento de Maiz Y Trigo) in Mexico and other locations where Heliothis species are being mass reared. Emphasized are techniques tor efficient rearing—establishment of the insect colony, the rearing facility, diet—and artificial infestation in screening and im• proving host-plant resistance to H. zea in maize. These techniques show promise of being adaptable to other pest species, crop species, and screening /breeding initiatives in other parts of the world. Finally, methods of efficient field infestation and rating scales used to evaluate ultimate damage and genotype resistance reactions are described.

The practice of growing varieties, lines, or hybrids cycles or generations of population improvement resistant to attack by insects, and their subsequent (Guthrie 1974, 1980). effectiveness in reducing pest populations and T h e basic c o m p o n e n t s necessary to identify or corresponding crop losses, is well documented for develop germplasm with resistance, or with higher several agricultural c r o p s a n d pest species. levels of resistance than cultivars n o w utilized, T h e d e v e l o p m e n t of many of these resistant c u l - include: tivars has resulted from or been facilitated by (1) m a n y years of study of the insect pests, (2) the 1. A colony of the insect species that exhibits the d e v e l o p m e n t of t e c h n i q u e s to m a s s rear the vigor and vitality of the damaging pest population insects, artificially infest, and screen the germ- within the geographical area that is affected. plasm of the crop species (or their wild relatives) for 2. T h e capability to efficiently m a s s culture the resistance, and (3) the successful application of pest species, including: rearing facility; trained per• appropriate breeding procedures for improvement sonnel; natural, meridic, or defined diets; and rear• of the resistance characteristic over succeeding ing procedures and containers. 3. Germplasm resources that are representative of

*Centro Internacional de Mejoramiento de Maiz Y Trigo (CIM- the genetic variation within the crop and/or its MYT), Mexico Cily, Mexico. closely related species.

International Crops Research Institute for the Semi-Arid Tropics. 1982 Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. 2 5 5 4. Methods of uniform artificial infestation. other pest species, crop species, and screening/ 5. Methods of assessing resultant damage, or breeding initiatives in other parts of the world. absence thereof, to the plants subjected to deliber• These techniques include the establishment of ate infestation (rating scales to determine classes the insect colony and basic requirements for effi• or categories of resistance or susceptibility). cient mass rearing. The latter focuses on the rear• 6. Screening, to determine whether adequate lev• ing facility, diet, and rearing containers, and on the els of resistance exist within suitable agronomic rearing procedures for the various life stages of types (equivalent or better than currently grown Heliothis zea. cultivars), and an effective selection/breeding The paper goes on to explain a method of effi• scheme established to improve either the resist• cient field infestation and concludes with a descrip• ance levels or the agronomic characteristics of the tion of the rating scales used to evaluate resultant "improved" materials. damage, which aids in the identification of resistant genotypes. This paper will present the experience accumu• lated and techniques developed at CIMMYT over the past 6 years for efficient mass rearing and Establishment of the Insect Colony infestation in screening and improving host-plant resistance to the corn earworm, Heliothis zea ( B o d - Guidelines established and recommended by die), in maize. (Fig. 1 a shows the species, of Helio- some entomologists who have developed crop cul• this occurring in Mexico.) The techniques tivars with resistance (Guthrie 1980), and proven described show promise of being adaptable to by experience under CIMMYT conditions, are fol• lowed to maintain a healthy, vigorous H. zea colony. As there is only one crop and infestation cycle per year in the tropical highlands of Mexico, the earworm colony is replaced, or rejuvenated, by Heliothis virescens using: (1) progeny of larvae collected from a late- Apatzingan, Mich. planted trap crop of sweet corn (Fig. 1b), or (2) 1 9 7 4 progeny of adults captured in a light trap in spring at the beginning of the rainy season (Fig. 1c). The colony is replaced or genetically mixed with wild stock at least every ten generations.

Heliothis subflexa Zacatepec, Mor. 1 9 7 4

Heliothis zea Chapingo,Mex. 1 9 7 4

Heliothis virescens Hermosillo, Son. 1974

Figure 1b. Collecting H. zea larvae in late- Figure 1a. Species of Heliothis occurring in planted sweet corn trap crop for establishing Mexico. the laboratory colony.

256 Leppla and Ashley (1978) have compiled a valua• ble reference on the types of physical facilities that are at present being used for insect rearing—from small chambers to grand-scale, semiautomated production. Anyone contemplating starting or expanding rearing programs should consult this reference for ideas that may apply to their particu• lar conditions. The physical facility should be simple, practical, and functional. Entomologists with experience in rearing the insect or species desired or contem• plated should be involved in the design or modifica• tion of the facility as applicable to their situation. If the entomologist has not had a great deal of expe• rience in mass rearing the species of concern, he should visit one or more facilities where the species are being successfully reared. In most cases, he will get new ideas; he should, however, be aware that everything he observes may not be approp• riate for his conditions, and that he may need to modify or adapt existing techniques to his o w n circumstances. The rearing facility that serves the CIMMYT maize program is a simple, inexpensive structure that satisfies the most basic requirements for insect rearing. It has been modified as necessary, Figure 1c. Light trap for collecting H. zea adults and this process is expected to continue. Most of for laboratory colony establishment or the changes made since its establishment have renovation. been to improve general sanitation and storage facilities, and to make it more independent of the other facilities. Efficient Mass Rearing In our experience, where we are producing four of the Insects or five species twice a year for field infestation at appropriate plant-growth stages over 2-month- long periods, insect rearing is a 7-day-a-week job. The basic requirements for successful insect Therefore, the laboratory must be independent of colonization and rearing were listed by Needham et other units, which operate only five or six days per al. (1937) and include: (1)food, (2) protection from week. This includes separate facilities for electrical enemies, (3) a suitable physical environment, and power, refrigeration, water, storage space, and (4) conditions suitable for reproduction general supplies. The components necessary in an efficient mass- One essential component in the CIMMYT facility, rearing operation include (1) the physical facility (2) which many rearing facilities do not have, is a small diet(s), (3) rearing containers, (4) rearing proce• workshop, with the necessary tools and materials dures, or management of the various life stages of for basic maintenance and for the construction of the insect, and (5) qualified trained personnel. rearing dishes, cages, or any unexpected necessi• ties. I am convinced that this small workshop has Rearing Facilities considerably improved the efficiency of our operation.

In many countries, physical facilities may consist simply of a r o o m or two, a few boxes and cages, Diet electrical power, and perhaps some means of temperature and humidity control. Some of the Singh (1977) lists seven meridic diets that have most developed countries have insect "factories." been used successfully for rearing H. armigera

257 (Hubner), and 16 diets that have been used for The diet register used at CIMMYT for preparing either H. virescens (Fabricius) or H. zea (Boddie), corn earworm diet is presented in Figure 2a. Use of or both. The adults of these Heliothis s p e c i e s are the checklist-register is recommended in order to illustrated in Figure 1 a. avoid errors in diet preparation, and for use as a

Amount I n g r e d i e n t to m a k e 10 k g d i e t 1 Water 8 l t d

2 A g a r 100 g

3 Soybean meal 500 g Ground opaque 9 6 0 g 4 m a i z e Brewer s or 4 0 0 g 5 Turula yeast 6 W h e a t germ 40 g 7 Sorbic acid 20 g

8 Choline chloride 20 g 9 Ascorbic acid 40 g Methyl p-Hydro- 2 5 g 10 x y b e n o a t e 11 Salt mixture W 7 0 g 12 Vitamin mixture 1 5 0 ml

13 Formaldehyde 2 5 ml 14 A u r e o m y c i n 50 g 15 Streptomycin 1 unit Maize tassel powder 16 (autoclaved) 200 g 17 O t h e r i n g r e d i e n t s if u s e d 18

Figure 2a. Diet preparation register tor corn earworm, Heliothis zea.

2 5 8 record to identify material lots that may coincide Rearing Containers with problems encountered in rearing. The only item unique to this diet is dried, sterilized, maize Containers suitable for rearing Heliothis spp cover tassel powder, added at the rate of 20 g/kg of diet. a wide range: individual glass or plastic vials or (The tassel is collected and processed prior to cups (Sparks and Harrell 1976), Hexcel units (Rob- pollen shed.) In tests under our conditions, we erson and Noble 1968; Raulston and Lingren obtained better larval establishment, shorter larval 1969), polystyrene light-diffusion cell blocks (Raul• period, larger pupae, and better oviposition from ston and Lingren 1972), and cell webs processed insects reared on diet with tassel powder than with • and infested by a modified Inline form-fill-seal out the powder on the standard diet. machine (Sparks and Harrell 1976). Guthrie et al. (1969) found that Ostrinia nubilalis Any of these may be utilized efficiently in a mass- larvae could survive to pupal stage on only maize rearing program, Choice may be dictated by the pollen, indicating that it is a nutritious food source. size of the rearing operation, cost and amount of Our trials at CIMMYT indicate that it acts as a labor available, and supply, availability, and dura• feeding stimulant and/or makes the diet more pal• bility of a given container. The ultimate and most atable. We have been using it in our diets for rearing efficient system would appear to be the Inline form - five lepidopterous species, with consistently good fill-seal machine and system (Sparks and Harrell results for the past 4 years. At CIMMYT, where the 1976). However, at CIMMYT and many other loca• crop is continually undergoing improvement, the tions in the world, it is probably not the best cho i c e , tassel powder is a low-cost diet ingredient. because of the cost of the initial unit and subse• Prepared commercial diets for rearing Heliothis quent materials, and the problems likely to be spp are now available from several sources in the encountered in operation and maintenance. In fact, USA. Our experience with them, however, has because of high costs associated with such pro• shown that we need to add a few ingredients, duction, a study was done to see if H. zea could be mainly supplemental vitamins and microbial inhibi• produced more economically on maize plants in tors, to use them successfully in our rearing facility. field cages (Sparks et al. 1971). They have the advantage of saving time and effort At CIMMYT, we have adapted the system used in preparation, while providing the necessary qual• by Raulston and Lingren (1972) to meet our needs ity assurance. They are somewhat more costly (Figs. 2b, 2c, 3a, 3b). The cell grids are made from than other alternative diets, but as long as the cost: polystyrene light-diffusion louvers available in benefit ratio is acceptable, we continue to use Mexico, the boxes are made locally from 3 and 6 them. mm Plexiglas, the cap for the unit is a layer of paper Walker et al. (1966) list criteria for diet suitability: toweling, a 50-mesh bronze screen, and a sheet of (1) high larval survival, (2) vigorous adults with high the polystyrene grid, held in place by inexpensive reproductive capacity, (3) normal rate of larval development, (4) low-cost ingredients, (5) easy preparation from readily available ingredients of uniform quality, and (6) good keeping quality. No single diet, however, will measure up to all these criteria for mass rearing a given species under all Heliothis zea CEW conditions or at all locations. However, after testing several diets that have been used successfully by other scientists, and after experimenting with var• ious concentrations of ingredients, it is possible to develop a suitable diet for a particular location a n d its conditions. New information on diets, diet ingredients, sup• pliers, and rearing techniques is available in the FRASS Newsletter (Anonymous 1981), published Spodoptera frugiperda FAW biannually by the Insect Rearing Group, which is composed of 575 scientists involved in rearing insects in 27 countries. It is provided free of cha r g e Figure 2b. Simple, locally made container for to interested scientists and is a valuable reference. rearing H. zea.

2 5 9 Figure 2c. A mixture of sterilized corncob grits and first-instar H. z e a larvae is applied to the Figure 3b. Pupae are manually removed from rearing container until there are approximately larval rearing containers and placed in simple five larvae per cell in the grid. screen cages for adult emergence.

Rearing Procedures and Colony Handling

Adult Stage

When we first began rearing H. zea at CIMMYT in 1975, we frequently lost our colonies b e c a u s e of sterility. Callahan (1962) reported that a major problem in rearing H. zea was unpredictable mating in the laboratory; consequently, he obtained a higher incidence of mating using large cages con• taining host plants, with controlled temperature and humidity, and a 10% honey solution for adult nutrition. Since 1977, we have used a similar mating cage (Fig. 3c) with continued s u c c e s s . It consists of a 0.5 Figure 3a. Rearing container with mature lar• x 0.5 x 1.0 m Plexiglas c a g e with s c r e e n on t w o vae. As H. z e a are cannibalistic, only one larva sides for the moths to hang and rest easily. A pot survives per cell to population. containing several whorl-stage maize plants is placed within the cage. A dish containing cotton moistened with a 10% sugar solution is also pro• large rubber bands. To minimize problems with vided. Moths are left in the cage for 48 hours before microbial contamination, the units are sterilized by they are transferred to oviposition cages. soaking them in 10% sodium hypochlorite solution, Oviposition c a g e s used at C I M M Y T consist of a and the boxes and grid blocks are surface-treated simple wire-frame support and a bag of nylon mesh by spraying with a 5% sorbic acid/5% methyl par- (Bridal Illusion) material (Fig. 4a). We find this sys• aben alcohol solution. This treatment does not tem superior to cotton cheese cloth placed over affect insect growth and aids in confining any paper icecream cartons (Burton 1969; Raulston chance contamination to a few cells within the box. and Lingren 1972), or on the front or sides of other Hot diet is poured into the dishes, and the grids style cages (Callahan 1962; Knott et al. 1966). Its forced into the diet manually. To further reduce advantages include ease in changing oviposition microbial contamination, the unit is exposed to UV substrate without adults escaping, ease in clean• radiation prior to infesting. ing, maximum oviposition surface area; there is

2 6 0 also no need for cage liners and no problem with hatching larvae, since the entire cage walls are replaced daily. Changing the cage (Fig. 4b) is accomplished by simply placing a new bag over the mouth of the egg-laden one. As the egg-laden one is pulled off, the new one is pulled over the frame. A small plastic box, with cotton moistened with a 10% sugar solu• tion, is placed inside for food.

Egg Stage

Egg-laden bags are placed in a small, inexpensive portable washing machine and agitated for 2 to 3 minutes in a 0.2% sodium hypochlorite solution. Egg-laden water is then decanted onto a fine mesh screen, the eggs are immersed in a 10% sodium thiosulfate solution, and then rinsed with water. (See Figs. 4c-5c). Eggs are then washed onto a paper towel, the excess moisture is removed, and the eggs are placed inside plastic dishes for incubation. Once larvae have hatched (0-8 hours old), they can be stored in a refrigerator (at 10°C) for up to 5 days, or used immediately to reinfest diet or plants in the field.

Figure 3c. Pupal containers are placed inside a 0.5 x 0.5 x 1/m mating cage, with potted maize Larval Stage plants and 10% sugar solution for adult food. Adults are transferred to oviposition cages At CIMMYT, newly hatched larvae (<12 hours old) every 24-48 hours. are used for infesting diet to maintain the laboratory colony.

Figure 4a. Oviposition cages consist of a sim• ple wire frame support and a bag made of nylon Figure 4b. Cages are changed daily by placing mesh (bridal illusion). Females oviposit and at• a clean nylon bag over the mouth of the egg- tach single eggs to the mesh. laden one.

261 Figure 5b. Eggs are decanted onto paper towel• ling and placed in box for incubation. They hatch in 2 days at 30°C and 95% RH.

Figure 4c. Egg-laden bags are agitated for 2 minutes in a small portable washing machine containing a 0.2% solution of sodium hypoch• lorite to loosen the eggs from the mesh. Then the egg-bearing water is decanted on to a fine mesh screen.

Figure 5c. Newly-hatched larvae are mixed with corn cob grits for field infestation.

ranging from 20 to 32°C, depending on how quickly the next generation is needed. Depending on temperature, larvae mature and Figure 5a. The eggs are then rinsed under tap begin pupating in 18 to 30 days. The developmental water to wash off the sodium hypochlorite, then stage can be easily checked through the clear decanted into a graduated cylinder to estimate Plexiglas box, w h i c h is not o p e n e d until pupal production. There are approximately 2 000 stage. Only one larva per cell survives to pupate eggs/ml. (Fig. 3a). Other rearing programs (Raulston and Lingren 1972; Burton 1969; Sparks and Harrell 1976) use eggs for infesting diet and rearing con• Infestation of the rearing boxes is accomplished tainers because they are more appropriate to their easily and rapidly: 100-200 cc of sterilized corncob systems. grits are placed in the dish containing larvae; this is rotated gently to mix uniformly. The mixture is transferred to a simple shaker jar and shaken over Pupal Stage the boxes containing diet a n d cell grid unit until there are 2 to 5 larvae per cell (Fig. 2c). After Many rearing operations, particularly those where capping, the rearing boxes are moved to shelves in m u c h or all of the p r o c e d u r e is m e c h a n i z e d , have rearing rooms at 70 to 80% RH and temperatures developed various machines for pupal extraction

2 6 2 Figure 6a. Plants with fully emerged, fresh silks to be infested are tagged with date of infestation Figure 6b. About 10 larvae are applied per for later identification. This is done prior to plant. Within minutes, they move into the silk infestation to avoid dislodging the larval grits mass and begin attacking the developing maize mixture. ear.

(Raulston and Lingren 1972; Sparks and Harrell both eggs and larvae (newly hatched, second 1976; Harrell et al. 1968, 1974). instar, and third instar). Manual infestation (using a At CIMMYT, by modifying the polystyrene cell camel's-hair brush) with newly hatched larvae was units into a split unit (three layers glued and one made over 40 years ago (Blanchard et al. 1942), layer below), we eliminated the need for any spe• and found to be an effective method (Josephson et cial machine for pupal collection, as nearly all al. 1966), but very inefficient because of the time pupae are found below the surface of the diet in our and labor involved. boxes. The split cell unit, when removed, splits the More efficient methods in use today include: (1) diet layer and pupation cell so that the pupae can infesting with eggs suspended in a 0.2% agar solu• be gently dumped from the dish. If desired, the few tion, applied to the plants in controlled amounts remaining pupae that pupated above the diet plug (hypodermic syringes or pressure applicators) or can be removed by hand or simply discarded. uncontrolled amounts (squeeze bottles) (Wiseman Pupae are placed one layer deep in boxes or et al. 1974); (2) infesting with uniform numbers of dishes of various sizes, depending on quantities, newly hatched larvae, using the Bazooka applica• and provided with a screen for newly emerged tor. The second technique was developed by Mihm adults to hang and spread their wings (Fig. 3b). and colleagues at CIMMYT in 1976 (CIMMYT These containers are then put inside the mating 1977). The technique and its advantages for use cages when the first adults have emerged (Fig. 3c). with several lepidopterous species were described in detail by Ortega et al. 1980. Infestation of maize Efficient Field Infestations with H. zea larvae is illustrated in Figures 6a and 6b. Larval infestation is more efficient than other Infestations with Heliothis spp have been done with means, because it is more rapid, uses less insects

263 per plant, and is more effective (fewer plants escape) than other techniques. To my knowledge, the Bazooka, in original or modified versions (Wise- man et al. 1980), has been used efficiently and effectively for field infestation with at least 11 species of lepidopterous insect larvae (Diatraea sac- charalis, D. grandiosella, D. lineolata, Ostrinia nubilalis, Chilo partellus, Sesamia cretica, S, cala- mistis. Busseola fusca, Heliothis zea, H. virescens, a n d Spodoptera frugiperda) a n d o n e leaf hopper (Dalbulus maidis) in three crop s p e c i e s — c o r n , Figure 7a. After deliberate infestation, plants s o r g h u m , a n d cotton. To use the t e c h n i q u e in cot• may be categorized as susceptible, interme• ton, the plants were simply sprayed first with water diate, or resistant. (Hall et al. 1980). If done after rain or heavy dew, infestations in cotton w o u l d be e v e n m o r e efficient, as spraying the plants w o u l d t h e n be unnecessary. REVISED CENTIMETER SCALE FOR CLASSIFYING For infesting c o r n or s o r g h u m in the whorl stages, CORN EARWORM DAMAGE TO MAIZE. (Widstrom 1967) the larval-corncob grits mixture is simply d i s p e n s e d into the whorl. For infesting developing CATEGORY VALUE DESCRIPTION maize ears, the mixture is d i s p e n s e d onto the fresh RESISTANT 0 No damage silks. For infesting sorghum near flowering stage, 1 Damage to silks only the mixture is d i s p e n s e d onto the panicle. Care must be t a k e n not to disturb the plant for a few 2 Feeding to 1 cm minutes after infestation, however, so that the lar• beyond the ear tip vae have time to attach themselves. INTERMEDIATE 3 . . . Value increases by If corncob grits are not readily available, other 1 for each additional centimeter of feeding materials m a y be u s e d in preparing the larval mix• beyond the tip ture. To my knowledge, corn meal (Hall et al. 1980), of the ear millet seed (personal communication), and SUSCEPTIBLE . . N s o r g h u m meal have been used successfully. Other materials will probably be reported as they are tried. Figure 7b. Use of the revised centimeter scale helps classify more exactly the plant reaction in screening and selecting in variable or segregat• Damage Evaluation ing maize genotypes.

Rating scales are generally used to quantify the resistance (or susceptibility) (Fig. 7a) of the plant(s) after infestation in the field or greenhouse. For c o r n e a r w o r m d a m a g e in whorl-stage c o r n , a scale similar to the o n e devised by W i s e m a n et al. (1976) is generally used. It is a 0 to 10 scale, where 0 is no d a m a g e a n d 10 is a completely destroyed plant. For d a m a g e to ears, the revised centimeter scale (Figs. 7b, 7c) developed by Widstrom (1967) is r e c o m m e n d e d as the most effective in indicating plants with heritable resistance.

Conclusion

The CIMMYT techniques and experience described in this paper for efficient mass rearing and Figure 7c. This ear shows an intermediate to infestation show promise oi adaptability to other susceptible reaction.

264 pest a n d c r o p species a n d to s c r e e n i n g a n d b r e e d • SPARKS, A.N. 1968. Collecting corn earworm pupae ing initiatives in other parts of the world. T h e final from rearing containers. U.S. Department of Agricul t u r e , objective in the application of these t e c h n i q u e s to Publication 42-160, Washington DC, USA. any program of efficient mass rearing and infesta• HARRELL, E.A., SPARKS, A.N., and PERKINS, W.D. tion is to identify resistant g e n o t y p e s for immediate 1974. Machine for collecting corn earworm pupae. U.S. use or for use in a breeding program. Varieties with Department of Agriculture, Agricultural Research Se r v i c e improved resistance c a n serve as o n e of the major Publication 5-43. 4 pp. c o m p o n e n t s in the effort to m a n a g e the Heliothis JOSEPHSON, L.M., BENNETT, S.E., and BURGES, spp pest populations. E.E. 1966. Methods of artificially infesting corn with the corn earworm and factors influencing resistance. Jo u r n a l of Economic Entomology 59:322-1234. References KNOTT, CM., LAWSON, F.R., and HOBGOOD, J.M. 1 9 6 6 . Oviposition cage for the tobacco budworm and the corn earworm. Journal of Economic Entomology 59:129 0 . ANONYMOUS. 1981. The Frass Newsletter. Insect Rearing Group (of the Society of America). Membersh i p LEPPLA, N.C., and ASHLEY, T.R. (eds). 1978. Facili• list address: R. Wheeler, Chevron Chemical Corp., 9 4 0 ties for insect research and production. U.S. Depar t m e n t Hensley St.. Richmond. Calif, 94804, USA. of Agriculture SEA Technical Bulletin 1576, Washingt o n , DC, USA. BLANCHARD, R.A., SATTERTHWAIT, A.F., and SNELLING, R.O. 1942. Manual infestation of corn LEPPLA, N.C., CARLYLE, S.L., GREEN, C.W., and strains as a method of determining differential ear w o r m PONS, W.J. 1978. Custom insect-rearing facility. Pages damage. Journal of Economic Entomology 35.508-511. 66-70 in Facilities tor insect research and product i o n , e d s N.C. Leppla and T.R. Ashley. U.S. Department of BURTON, R.L. 1969. Mass rearing the corn earworm in Agriculture—SEA Technical Bulletin 1576. 86 pp. the laboratory. U.S. Department of Agriculture, Agr i c u l t u • ral Research Service Publication 33-134, Washington NEEDHAM, J.G, GALTSOFF, P.S., LUTZ, F.W., and DC, USA. 8 pp. WELCH, P.S. (eds.). 1937. Culture methods for inverte• brate animals. Comstock, NY. Reprinted 1959. New York, CALLAHAN, P.S. 1962. Techniques for rearing the corn USA: Dover Publications. e a r w o r m , Heliothis zea. Journal of Economic Entomology 55:453-457. ORTEGA, A., VASAL, S.K., MIHM, J., and HERSHEY, C. 1980. Breeding for insect resistance in maize. Pages CIMMYT (Centro Internacional de Mejoramiento de 371 -419, in Breeding plants resistant to insects (eds. F.G. Maiz y Trigo). 1977. CIMMYT Review 1977. El Batan, Maxwell and PR. Jennings). New York. USA: John Wiley. Mexico, 99 pp. RAULSTON, J.R., and LINGREN, P.D. 1969. A t e c h • GUTHRIE, W.D. 1974. Techniques, accomplishments nique for rearing larvae of the bollworm and tobacc o and future potential of breeding for resistance to E u r o • budworm in large numbers. Journal of Economic Ento• pean corn borer in corn. Pages 359-380 in Proceedings, mology 62:959-961. Summer Institute on Biological Control of Plant Ins e c t s and Diseases eds K.G. Maxwell and FA. Harris. Univer• RAULSTON, J.R., and LINGREN, P.D. 1979. M e t h o d s sity of Mississippi press, Jackson, Miss, USA. of large-scale rearing of the tobacco budworm. U.S. Department of Agriculture. Production Research Repo r t GUTHRIE, W.D. 1980. Breeding for resistance to No. 145, Washington, DC, USA 10 pp. insects in corn. Page 290 in Biology and breeding for resistance to arthropods and pathogens in agricultu r a l ROBERTSON, J.L., and NOBLE, L.W. 1968. Rearing of plants, ed. M.K. Harris. Proceedings, International Short tobacco budworm in honey comb-like cells. Journal o f Course in Host-Plant Resistance, Texas, A & M Univer• Economic Entomology 61:331 -332. sity, College Station, Texas, USA. 605 pp. SINGH, P. 1971. Artificial diets for insects, mites and GUTHRIE, W.D., HUGGANS, J.L., and CHATTERJI, spiders. New York, USA: Plenum. 594 pp. S . M . 1 9 6 9 . Influence of corn pollen on the survival and SPARKS, A.N., and HARRELL, E.A. 1976. C o r n e a r - development of second-brood larvae of the European worm rearing mechanization. U.S. Department of Agri c u l • corn borer. Iowa State Journal of Science 44:185-19 2 . ture, Agricultural Research Service Technical Bulletin HALL, P.K., PARROT, W.L., JENNINGS, J.N., and 1554.11 pp. McCARTY, J.C. 1980. Use of tobaco budworm eggs SPARKS, A.N., WISEMAN, B.R., and McMILLIAN, and larvae for establishing field infestations on c o t t o n . W . W . 1 9 7 1 . Production of corn earworms on several Journal of Economic Entomology 73:393-395. hosts in field cages. Journal of Economic Entomolog y HARRELL, E.A., BURTON, R.L., HARE, W.W., a n d 64:540-541.

2 6 5 WALKER, D.W., ALEMANY, A., QUINTANA, V., PADOVANI, F., and KAGEN, K.S. 1966. I m p r o v e d xenic diets for rearing the sugarcane borer in Puerto R i c o . Journal of Economic Entomology 59(1 ):1 -4.

WIDSTROM, N.W. 1967. An evaluation of methods for measuring corn earworm injury. Journal of Economic Entomology 60:791 -794.

WISEMAN, B.R., WIDSTROM,N.W., and McMILLIAN, W . W . 1974. Methods of application and numbers of eggs of the corn earworm required to infest ears of corn artifi• cially. Journal of Economic Entomology 67:74-76.

WISEMAN, B.R., WIDSTROM, N.W., McMILLIAN, W.W., and PERKINS, W.D. 1976. Greenhouse evalua• tions of leaf-feeding resistance in corn to corn ea r w o r m (Lep. Noct). Journal of the Georgia Entomological Society 11:63-67.

WISEMAN, B.R., DAVIS, F.M., and CAMPBELL, J.E. 1 9 8 0 . Mechanical infestation device used in fall armyworm plant resistance programs. Florida Entomologis t 63(4):425-432.

2 6 6 Screening Groundnut for Heliothis Resistance

W.V. Campbell, J.C. Wynne, and H.T. Stalker*

Abstract

Plant introductions, commercial cultivars, and groundnut breeding lines were screened in the field for resistance to Heliothis zea, using naturally occurring populations of the pest. Plant introductions from South America were generally susceptible. PI-269062 from China exhibited resistance to H. zea. NC-6 (NC-343 x Va-61 R), which was developed tor resistance to the southern corn rootworm, was cross-resistant to H. zea. The sister lines, NC-GP 343 and NC-AC 342 were also resistant. Some wild species of groundnut in the sections Arachis, Erectoides, Rhizomatosae, Ambinervosae, Caulorhizae, Extranervosae and Triseminalae exhibited high resistance, and some approached immunity to H. zea. Nonpreference and antibiosis were identified as mechanisms of resistance. Larval weight was reduced three- to five-fold on resistant cultivated groundnuts and 700% mortality resulted when larvae were fed some wild species. The low to moderate level of resistance present in the cultivated groundnut is of econom• ic importance in a pest-management program. Generally the resistant cultivars and breeding lines will maintain H. zea below the damage threshold.

G r o u n d n u t (Arachis hypogaea L.) is attacked by a Defoliation from H. zea occurs principally during complex of insects and mites. Among these pests August (90 to 130 days postplant). Larval feeding the corn earworm Heliothis zea (Boddie) has coincides with the period of principal fruit produc• recently become an economic pest. Prior to 1977, tion. Defoliation during this critical period of gro w t h H. zea damage to groundnut was subeconomic in has the greatest effect on reducing yield (Camp• North Carolina, but recently 50% or higher defolia• bell, unpublished). tion has been observed. Pesticides applied in North Carolina during August to control H. zea often result in adverse interactions that induce spider-mite outbreaks. Any *North Carolina State University, Raleigh, NC. USA, pesticide that does not have miticidal properties

Journal Series Paper 8079, North Carolina Agricultural Research may cause an increase in the population of the Service. Raleigh, NC, USA. two-spotted spider mite, Tetranychus urticae,

C u l t i v a r o r A v e r a g e plant introduction L o c a t i o n defoliation (%)

F l o r i g i a n t 1 2 . 5 N C 2 1 0 . 0 N C 5 9 . 0 N C 6 6 . 0 N C - G P 3 4 3 1 1 . 0 N C - 1 5 7 2 9 1 0 . 0 N C - 1 0 2 7 2 7 . 5 N C - 1 5 7 4 5 8 . 5 N C - 1 0 2 4 7 9 . 0 PI-261959 Violaceo I P a r a g u a y 2 4 . 0 Pl-261924 Negro I A r g e n t i n a 1 0 . 0 PI-261931 Palido I P a r a g u a y 1 8 . 0 PI-261940 Colorado 1 P a r a g u a y 1 3 . 5 PI-261965 Violaceo I P a r a g u a y 1 2 . 5 PI-261929 Negro I A r g e n t i n a 2 4 . 0 PI-261938 Colorado I P a r a g u a y 2 1 . 5 Pl-261968 Violaceo I P a r a g u a y 1 7 . 5 PI-261951 Colorado I P a r a g u a y 1 6 . 0 PI-261935 Palido l P a r a g u a y 1 1 . 5 Pl-275696 Palido II Goias, Brazil 1 3 . 5 PI-262052 Colorado l Sao Paulo, Brazil 2 4 . 0 P I - 2 6 9 0 6 2 C h i n a 4 . 5 PI-268768 Super Khandeish from Jozi collection, Sudan 1 4 . 0 PI-268740 B727 (sequential) R h o d e s i a 1 6 . 5 PI-270804 Nalal ex-NC-46 R h o d e s i a 1 8 . 5 PI-271023 Spanish (alternate) R h o d e s i a 1 8 . 5 PI-270901 Manyuna (alternate) R h o d e s i a 1 4 . 0 PI-275691 Manyuna (alternate) II Goias, Brazil 1 5 . 0 PI-275728 S.L. Jater II Goias, Brazil 1 3 . 5 PI-270853 Ndala Bunch R h o d e s i a 1 6 . 5 PI-275742 S.S. 16 M i n a s G e r a i s , B r a z i l 2 2 . 5 PI-262042 Palido I Sao Paulo, Brazil 2 1 . 0 PI-270764 Short Valencia ex EC I R h o d e s i a 1 5 . 0 P I - 2 7 5 7 5 3 2 1 . 0 PI-275735 S.S. 181 II M i n a s G e r a i s , B r a z i l 1 5 . 0 PI-270803 Pink ex BC 259 R h o d e s i a 1 8 . 5 PI-275719 II M i n a s G e r a i s , B r a z i l 1 5 . 0 PI-262095 Colorado IV B o l i v i a 1 9 . 0 PI-275700 II M i n a s G e r a i s , B r a z i l 1 6 . 5 PI-262031 Colorado I Sao Paulo, Brazil 1 8 . 0 PI-271014 Valencia Rouge de R h o d e s i a 1 6 . 5 PI-270773 White Manyuna Cordoba R h o d e s i a 1 6 . 0 PI-269006 S-726 (alternate runner) R h o d e s i a 1 1 . 5 PI-262060 Colorado I S a o P a u l o 1 6 . 0 PI-262069 Palido I S a o P a u l o 1 9 . 0 Pl-275687 II M i n a s G e r a i s , B r a z i l 1 4 . 5 P I - 2 7 4 2 6 7 1 3 . 5 PI-262080 Colorado I Mato Grosso, Brazil 1 9 . 0 PI-269049 Ndoba NCR-2 Rhodesia (alternate runner) 1 5 . 0 PI-270792 Brown ex-BC 253 R h o d e s i a 1 8 . 0

L S D ( 0 . 0 5 ) 7 . 3

2 6 8 K o c h , on groundnut in North Carolina ( C a m p b e l l d a m a g e (Table 1). PI-269062 exhibited the lowest 1978). defoliation; the next lowest being NC-6, a North An ideal solution to the control of H. zea w o u l d be Carolina cultivar selected from the cross of N C - G P the development of groundnut cultivars with resist• 343 and Va-61 R that has multiple insect resistance a n c e to H. zea. S u c h resistance has b e e n reported (Campbell and Wynne 1980). All but five plant intro• for several other crops, including sweet corn (Brett ductions exhibited significantly higher H. zea d a m • 1958), field c o r n (Douglas a n d Eckhardt 1957; age than N C - 6 . McMillian a n d W i s e m a n 1972), s o y b e a n s (Clark et Groundnut breeding lines, including selections al. 1972), and cotton (Lukefahr et al. 1965). Numer• from crosses involving NC-6, which is moderately ous other references of Heliothis resistance in c r o p resistant to H. zea (Campbell a n d W y n n e 1979), plants are f o u n d in the c o m p r e h e n s i v e review by s h o w e d significant differences in d a m a g e from H. Maxwell et al. (1972). zea. NC-6 and NC-GP 343, the insect-resistant However, information on resistance of groundnut parent of NC-6, had less defoliation than Florigiant. to H. zea is limited. Leuck et al. (1967) reported that Breeding lines that showed less than 8% defoliation Spanish cultivars were more susceptible than Vir• included 17168 x N C - 6 , N C - 6 x 17164, 17168 x ginia cultivars. C v s Florigiant and Virginia B u n c h 15753, and 15753 x 17163 (Table 2). Resistance in had the lowest damage, but differences in H. zea most of these breeding lines resulted from the use d a m a g e were not significant a m o n g the Virginia of N C - G P 343 or N C - A C 342 as parents. types. When tested in advanced generations, NC-6, NC-Ac 342, and NC-GP 343 (insect-resistant sis• ter lines) and crosses containing N C - A c 342 a n d Field Screening Groundnut N C - G P 343 generally exhibited less H. zea defolia• for H. zea Resistance tion than the susceptible Florigiant c h e c k (Table 3). The lowest damage was in a selection from the Evaluation of germplasm was not initiated in North cross of N C - G P 3 4 3 x Florigiant. Carolina until 1977, b e c a u s e of the low H. zea An additional evaluation of cultivars and populations prior to this time. Groundnut was selected breeding lines for H. zea resistance in planted in single, 1 0 - m rows a n d replicated three 1977 a n d 1978 s h o w e d the following cultivars had times. C o r n is rotated with groundnut, a n d approxi• less defoliation than Florigiant: N C - 6 , NC-FIa 14, mately 4 0 % of the area w h e r e the experiment w a s Va-72R, NC-5, Florunner, and Early Bunch. A c o n d u c t e d was planted in c o r n e a c h year. This breeding line selected from the cross of Florigiant provided a local population of H. zea e m e r g i n g from and a Valencia PI received the highest damage corn. No effort has been m a d e to s u p p l e m e n t natu• (Table 4). rally o c c u r i n g field populations of H. zea. H. zea population pressure was highest in 1980. Egg laying o c c u r s over a period of 3 to 5 w e e k s , Under high populations of H. zea, N C - 6 , the resist• generally starting in early August (90 days post- ant sister lines N C - A c 342 a n d N C - G P 343, piant). Where H. zea d a m a g e is low, groundnut c r o s s e s containing these lines, a n d Early B u n c h lines may be evaluated by counting the n u m b e r of sustained less defoliation than Florigiant. NC-6 had d a m a g e d leaves, but w h e r e d a m a g e is high, this is 6.7% defoliation and Early B u n c h , 12%, while Flori• not possible. In such cases, determining defoliation giant had 46.7% defoliation (Table 5). is a better m e t h o d of rating lines suffering extensive Breeding lines that have been tested for a d a m a g e . In North Carolina, defoliation is rated on a number of years and lines that are agronomically 0 to 1 0 0 % scale, but alternative d a m a g e - r a t i n g promising for release were evaluated in an experi• scales of 0 to 9 or 0 to 5 may be used w h e r e the ment called Advanced Test. Using NC-6 as the numbers progressively represent light, moderate, standard resistant line and Florigiant as the stand• heavy, severe, and total defoliation. Generally, ard susceptible line, only 8 entries a m o n g the 48 plots are visually rated for percent defoliation in tested s h o w e d defoliation equal to or less t h a n early S e p t e m b e r a n d after peak H. zea damage. It is N C - 6 . A m o n g the entries with low d a m a g e from H. important to observe the entire row, b e c a u s e of zea were NC-6, NC-17404, NC-GP 343 x Florigiant, variation in d a m a g e within the row. ( N C - G P 343 x N C - 5 ) x UF 7 0 1 1 5 , G K - 3 x U F - In 1977 a g r o u p of plant introductions w e r e c o m • 70115, a n d PI-138870 x N C - 5 (Table 6). p a r e d with four North Carolina cultivars a n d five NC-6 (multiple insect-resistant cultivar) was potato leafhopper resistant accessions for H. zea crossed with NC-3033 (Cylindrocladium black rot

2 6 9 Table 2. Resistance of F8 groundnut lines to Heliothis Table 3. Resistance of F1 2 groundnut Unas to Helio- Mm, North Carolina, USA, 1977. t h i s zea, North Carolina, USA, 1978.

Breeding line A v e r a g e Breeding line A v e r a g e or cultivara defoliation or cultivara defoliation (%) (%)

NC-GP 343 x Florigiant 1 . 7 N C - A c 1 7 1 6 8 x N C - 6 6 . 5 NC-GP 343 x Florigiant 6 . 0 N C - A c 1 7 1 6 8 x N C - 6 1 0 . 0 F l o r i g i a n t x N C - A c 3 4 2 4 . 3 N C - A c 1 7 1 6 6 x N C - A c 1 5 7 5 3 1 1 . 0 N C - A c 3 0 1 x N C - 5 7 . 0 N C - 6 x N C - A c 1 7 1 6 4 1 2 . 0 N C - G P 3 4 3 x N C - 5 3 . 0 N C - 6 x N C - A c 1 7 1 6 4 7 . 0 NC-GP 343 x Florigiant 1 2 . 3 N C - A c 1 7 1 6 3 x N C - A c 1 7 1 6 8 1 7 . 5 N C - G P 3 4 3 x N C - 2 6 . 3 ' F l o r i g i a n t 1 3 . 5 F l o r i g i a n t x N C - A c 3 4 2 8 . 0 N C - A c 1 7 1 6 3 x N C - A c 1 7 1 6 6 1 4 . 5 N C - A c 3 0 1 x V a - 6 1 R 7 . 3 N C - A c 1 7 1 6 3 x N C - 6 1 1 . 0 N C - A c 3 0 1 x N C - 2 4 . 7 N C - A c 1 7 1 6 3 x N C - 6 1 1 . 5 F l o r i g i a n t x N C - A c 3 0 1 1 0 . 7 N C - A c 1 7 1 6 8 x N C - A c 1 5 7 5 3 1 4 . 0 N C 5 x N C - A c 3 4 2 4 . 0 N C - A c 1 7 1 6 8 x N C - A c 1 5 7 5 3 7 . 0 NC-GP 343 x NC-5 5 . 0 N C - A c 1 7 1 6 8 x N C - A c 1 7 1 6 6 8 . 0 NC-GP 343 x Florigiant 1 8 . 7 N C - A c 1 7 1 6 4 x N C - A c 1 7 1 6 3 1 1 . 0 N C - A c 3 0 1 x N C - 5 7 . 0 N C - A c 1 7 1 6 4 x N C - A c 1 7 1 6 3 1 6 . 0 N C - A c 3 0 1 x N C - 2 7 . 7 N C - A c 1 5 7 5 3 x N C - A c 1 7 1 6 3 6 . 5 NC-Ac 302 x Florigiant 6 . 3 N C - A c 1 5 7 5 3 x N C - A c 1 7 1 6 3 7 . 5 N C - G P 3 4 3 x N C - 5 3 . 0 N C - A c 1 5 7 5 3 x N C - A c 1 7 1 6 3 1 8 . 0 NC-Ac 302 x Florigiant 1 3 . 7 NC-Ac 15753 x NC-Ac 17164 1 3 . 5 N C - A c 3 0 2 x N C - 2 6 . 3 N C - A c 1 5 7 5 3 x N C - A c 1 7 1 6 4 1 2 . 5 F l o r i g i a n t x N C - A c 3 0 1 1 5 . 7 N C - A c 1 5 7 5 3 x N C - A c 1 7 1 6 4 1 6 . 0 F l o r i g i a n t x N C - A c 3 0 1 4 . 3 N C - 6 5 . 0 F l o r i g i a n t x N C - A c 3 0 1 1 1 . 0 F l o r i g i a n t 1 6 . 0 N C - A c 3 0 1 x N C - 5 1 0 . 0 N C - G P 3 4 3 9 . 0 N C - A c 3 4 2 3 . 7 N C - G P 3 4 3 3 . 7 L S D ( 0 . 0 5 ) 5 . 5 N C - 6 2 . 3 F l o r i g i a n t 1 4 . 3

a . Pedigree of NC Accessions as follows: L S D ( 0 . 0 5 ) 4 . 9 Ac-15753 = selection from CVShulamit.

A c - 1 7 1 6 3 = N C - 5 x F l o r i g i a n t .

Ac-17164 = Florigiant x Fla-393- a . N C - G P 3 4 3 , N C - A c 3 4 2 , N C - A c 3 0 1 , a n d

Ac-17166 = Florigiant x Ac-342. NC-Ac 302 are sister lines selected from

A c - 1 7 1 6 8 = N C - 5 x A c - 3 4 2 . t h e c r o s s o f N C - B u n c h x P I - 1 2 1 0 6 7 .

resistant) and screened for insect resistance. All of istance of the two contrasting cultivars, Florigiant the NC-6 x NC-3033 lines selected for insect res• and NC-6. Plots were eight rows wide (1-m row istance exhibited damage in the range of the NC-6 spacing) and approximately 50 m long, with three parent (Table 7). These data indicate that H. zea replications. resistance is heritable. Furthermore the breeding Early-planted (May 7) groundnut had less H. zea lines gave similar reactions in 1979 and 1980. damage than late planted (May 23 and June 3), regardless of the cultivar tested. A May 23 planting had the highest foliage damage, suggesting opti• Effect of Planting Date mum synchronization of groundnut development with the moth flight. Florigiant was more suscepti• Three planting dates were employed to determine if ble over a wider range of planting dates than NC-6 date of planting influenced the susceptibility/res- (Table 8). Douglas (1954) and Luckman (1956)

2 7 0 Table 4. Resistance of groundnut cultivars and Table 5. Resistance of groundnut to Heliothis zea. breeding lines to Heliothis zea, North Carolina, USA. North Carolina, USA, 1980.

Breeding line Average defoliation (%) A v e r a g e Breeding line or cultivar 1 9 7 7 1 9 7 8 defoliation or cultivar (%)

N C - 2 1 8 . 0 7 . 3 N C - 2 2 4 . 3 N C - 4 1 4 . 0 1 . 7 N C - 5 2 7 . 0 N C - 5 1 3 . 3 3 . 3 F l o r i g i a n t 4 6 . 7 N C - 6 7 . 3 1 . 0 N C - 7 2 1 . 7 N C - 1 7 1 0 . 7 4 . 7 N C - 6 6 . 7 N C - F I a 1 4 7 . 7 NR Early Bunch 1 2 . 0 V a - 7 2 R 1 2 . 7 4 . 0 N C - 3 0 3 3 2 5 . 0 A v o c a - 1 1 1 5 . 0 5 . 7 N C - G P 3 4 3 1 4 . 0 S h u I a m i t 1 3 . 0 NR F l o r u n n e r 1 7 . 0 G K - 3 1 0 . 0 8 . 0 N C - A c 3 4 2 6 . 0 Early Bunch 4 . 7 NR Florigiant x Spanhoma 4 8 . 3 F l o r u n n e r 8 . 3 3 . 3 NC-GP 343 x Florigiant 1 1 . 3 N C - G P 3 4 3 NR 4 . 0 Florigiant x NC-Ac 342 1 3 . 3 N C - 3 0 3 3 2 4 . 0 1 0 . 7 N C - G P 3 4 3 x N C - 5 1 1 . 7 NC-6333 x NC-5 1 8 . 7 NR Florigiant x NC-Ac 301 1 0 . 7 NC-3033 x NC-2 1 8 . 3 NR NC-5 x NC-Ac 342 9 . 0 NC-5 x NC-7484 1 1 . 7 NR NC-GP 343 x NC 5 8 . 0 NC-5 x Fla-393 9 . 0 6 . 3 NC-GP 343 x Florigiant 3 4 . 3 Florigiant x Florunner 2 2 . 3 8 . 3 NC-Ac 301 x NC-5 1 6 . 0 Florigiant x Valenciaa 2 4 . 0 1 4 . 3 NC-Ac 301 x NC-5 1 7 . 3 F l o r i g i a n t 1 9 . 3 1 2 . 3 N C - G P 3 4 3 x N C - 5 9 . 3 NC-Ac 302 x Florigiant 2 9 . 0 L S D ( 0 . 0 5 ) 5 . 5 5 . 9 Florigiant x NC-Ac 301 3 0 . 0 NC-Ac 17168 x NC 6 3 0 . 0 a. PI-337396. NR = not recorded NC-Ac 17163 x NC-Ac 17166 3 3 . 3 NC-Ac 17163 x NC 6 1 2 . 3 NC-Ac 17164 x NC-Ac 17163 3 1 . 7 NC-Ac 15753 x NC-Ac 17163 5 3 . 3 NC-Ac 15753 x NC-Ac 17164 6 5 . 0 NC-Ac 15753 x NC-Ac 17164 2 6 . 7 f o u n d early-planted c o r n also h a d less d a m a g e NC-Ac 15753 x NC-Ac 17163 2 6 . 7 from H. zea, a n d Stinner et al. (1976) reported early- planted soybeans escaped H. zea d a m a g e . L S D ( 0 . 0 5 ) 1 2 . 2

Field Screening Wild Species

Greenhouse-grown seedlings of wild Arachis s p e • cies were transplanted in the field in single-row, six-plant plots. Three commercial cultivars were Laboratory Screening Groundnut u s e d as standards to c o m p a r e t h e reaction of Ara• for Resistance chis collections to H. zea. H. zea A m o n g the wild species, there is e v i d e n c e of high r e s i s t a n c e to H. zea that approaches immunity T h e m e c h a n i s m s of plant resistance to insects (Table 9). T h e r e w a s m o r e d a m a g e to the wild were p l a c e d in three categories by Painter (1951): s p e c i e s in 1981 t h a n in 1979 or 1980; however, nonpreference, antibiosis, a n d tolerance. We util- damage was still considerably less than that for the ized these categories to study the m e c h a n i s m of domestic cultivars. resistance to H. zea in groundnut.

271 Table 6. Resistance of groundnut to Heliothis zea, Table 7. Resistance of NC-6 x NC-3033 groundnut North Carolina, USA, 1981. lines to Heliothis zea, North Carolina, USA.

Breeding line A v g . % Breeding line Average defoliation (%) or cultivar defoliation or cultivar 1 9 7 9 1 9 8 0 F l o r i g i a n t 1 6 . 7 N C - 6 7 . 7 NC-6 x NC-3033 1 . 3 1 6 . 0 N C - 7 1 2 . 3 2 . 7 1 7 . 7 N C - 1 8 2 2 2 1 0 . 0 2 . 3 2 0 . 0 N C - 1 8 2 2 4 1 1 . 3 1 . 3 1 4 . 0 1 2 . 7 N C - 1 8 2 2 5 2 . 0 1 5 . 0 N C - 1 7 9 2 1 1 6 . 3 2 . 7 1 4 . 3 N C - 1 7 9 2 2 1 2 . 7 3 . 0 2 3 . 3 N C - 1 7 9 7 6 1 1 . 7 1.7 2 2 . 7 N C - 1 7 4 0 4 7 . 0 N C - 7 7 - 2 1 1 . 7 2 . 7 1 5 . 7 N C - 7 7 - 6 2 1 . 7 3 . 0 2 2 . 0 N C - 7 7 - 7 1 4 . 0 3 . 0 1 6 . 0 N C - 1 7 9 4 1 1 7 . 7 F l o r i g i a n t 7 . 3 5 0 . 0 N C - 3 1 3 9 1 2 . 3 N C - 6 1 . 3 1 9 . 3 V a - 7 1 - 3 4 7 1 4 . 0 N C - 2 9 . 0 3 2 . 3 NC-Ac 3139 x Florigiant 1 7 . 3 N C - 3 0 3 3 NR 2 8 . 3 NC-3033 x NC-2 1 1 . 3 N C - 7 NR 3 6 . 0 NC-GP 343 x Florigiant 7 . 3 Florigiant x NC-Ac 342 9 . 0 L S D ( 0 . 0 5 ) 2 . 2 7 . 3 N C - G P 3 4 3 x N C - 5 1 1 . 0 Florigiant x NC-Ac 301 1 4 . 7 NR = Not recorded. NC 5 x NC-Ac 342 1 1 . 7 N C - G P 3 4 3 x N C - 5 1 6 . 0 NC-GP 343 x Florigiant 1 0 . 7 NC-Ac 301 x NC-5 1 4 . 7 NC-Ac 301 x NC-5 1 2 . 3 Table 8. Effect of planting data and cultivar on He l i o - N C - G P 3 4 3 x N C - 5 9 . 7 t h i s zea damage to groundnut, North Carolina, USA, NC-Ac 302 x Florigiant 1 7 . 7 1 9 8 0 . Florigiant x NC-Ac 301 1 9 . 0 NC-Ac 17163 x NC-Ac 17166 1 5 . 3 Date of planting Average foliage NC-Ac 17164 x NC-Ac 17163 1 3 . 0 and cultivar d a m a g e NC-Ac 15753 x NC-Ac 17163 1 4 . 7 (%) NC-Ac 15753 x NC-Ac 17164 9 . 7 NC-Ac 15753 x NC-Ac 17164 1 6 . 0 NC-Ac 15753 x NC-Ac 17163 1 5 . 0 M a y 7 (NC x Fla 393) x PI-138870 1 3 . 0 N C - 6 6 . 7

(NC-GP 343 x Va-61R) x (B2 x N C - 4 ) 9 . 0 F l o r i g i a n t 1 4 . 0 (NC-GP 343 x NC-5) x UF-70115 1 0 . 0 (NC-GP 343 x NC-5) x UF-70115 6 . 0 M a y 2 3 (NC 5 x Florigiant) x (NC-5 x Fla-393) 1 4 . 0 N C - 6 1 5 . 0 UF-73307 x UF-73307 1 0 . 7 F l o r i g i a n t 4 1 . 0 GK-3 x (Florigiant x NC-Ac 342) 9 . 0 GK-3 x UF-70115 1 0 . 0 J u n e 3 GK-3 x UF-70115 3 . 3 N C - 6 6 . 3 GK-3 x UF-70115 5 . 3 F l o r i g i a n t 2 7 . 7 (B2 x NC-5) x Florigiant 1 6 . 3 (B x NC 5) x Florigiant 1 6 . 0 2 L S D ( 0 . 0 5 ) 6 . 3 PI-152122 x Frost resistant 1 2 . 3 PI-138870 x NC-5 1 5 . 0 PI-138870 x NC-5 7 . 3 PI-138870 x (B, x NC-4) 8 . 3 (Florigiant x NC-5) x Nonpreference (Florigiant x Valencia) 1 2 . 3

L S D ( 0 . 0 5 ) 6 . 7 Heliothis zea larvae normally do not h a v e a c h o i c e of host plants. In these tests, larvae w e r e provided a

2 7 2 T a b l e 9 . R e a c t i o n o f A r a c h i s collections to Heliothis zea in field tests, at Lewis ton, NC, USA.

M e a n n o . o f l e a v e s N o . o f No. of damaged leaves (avg. and range) d a m a g e d a S e c t i o n g e n o t y p e s 1979 1 9 8 0 1 9 8 1 1 9 7 9 - 1 9 8 1

Arachis 1 1 1 . 8 2 2 . 1 3 4 . 5 7 2 . 8 4 ( 0 . 4 - 5 . 0 ) ( 1 . 0 - 4 . 3 ) ( 1 . 0 - 6 . 3 ) Erectoides 6 1 . 5 0 1 . 5 5 3 . 7 8 2 . 2 8 ( 1 . 0 - 2 . 5 ) ( 2 . 0 - 5 . 7 ) ( 2 . 0 - 5 . 7 ) Rhizomatosae 2 1 1 . 6 0 0 . 8 0 1 2 . 0 5 4 . 8 1 ( 0 - 5 . 5 ) ( 0 - 1 . 7 ) ( 3 . 3 - 3 5 . 7 ) Ambinervosae 1 0 . 5 0 . 3 0 . 7 0 . 5 Caulorhizae 1 0 . 0 0 . 0 2 . 0 0 . 6 7 Extranervosae 1 2 . 5 1 . 3 3 . 3 2 . 3 7 Triseminalae 1 1.0 0 . 7 NR 0 . 8 5 C u l t i v a t e d c h e c k s : F l o r i g i a n t 1 3 . 5 4 0 . 0 6 0 . 0 3 7 . 8 3 N C - 2 1 4 . 0 2 6 . 0 5 1 . 7 3 0 . 5 7 N C - 6 4 . 5 1 0 . 0 3 0 . 0 1 4 . 8 3 a . Means are average of two replicates for 1979 and t hree replicates for 1980 and 1981.

N R = n o t r e c o r d e d .

choice of three cultivars to determine larval prefer• ence. An excised leaf from each of three cultivars T a b l e 1 0 . P r e f e r e n c e o f H e l i o t h i s z e e larvae for was placed in a petri dish with moist filter paper. groundnut cultivars, laboratory test, 1979. Nine 4-day-old larvae were released in the center a of each dish. Damage was determined 4 days after C u l t i v a r Average foliage damage larval release. (%) The larvae preferred NC-2 and Florigiant to NC-6 N C - 6 2 0 . 8 for feeding (Table 10). NC-6 received only half the N C - 2 4 4 . 0 damage of NC-2 and Florigiant. F l o r i g i a n t 4 4 . 5

L S D ( 0 . 0 5 ) 5 . 4

Antibiosis a . Each replicate infested with nine 4-day-old

larvae that fed for 4 days. The same three cultivars were tested for antibiosis, or the adverse effect of the plant on the normal metabolism of the insect. The experiment was con• ducted in an insect-rearing room, with plastic jelly cups (4-cm diameter and 4,5 cm deep) for cages. A In another test, NC-6 and one of the insect- and single 4-day-old, diet-reared larva was placed in disease-resistant breeding lines, NC-6 x 3033, each cup with sufficient excised groundnut leaflets were compared for effect of resistance on the for 1 day's food. Food was changed daily, and development of the insect. NC-6 and NC-6 x 3033 larvae were weighed when 10 days old. (selected line) did not differ from each other in their In Test 1 larvae reared on NC-2 and Florigiant effect on larval weight gain, days to pupation, or weighed approximately three times more than lar• emergence date; however, larvae reared on these vae reared on NC-6. In Test 2 larvae weighed three two lines weighed less, pupated later, and emerged times and five times more when reared on NC-2 later than those reared on NC-2 and Florigiant and Florigiant, respectively, than when reared on (Table 12). Beland and Hatchett (1976) reported H. NC-6 (Table 11). zea pupated 3 to 5 days earlier on susceptible

2 7 3 s o y b e a n lines t h a n on the resistant s o y b e a n intro• r e p l a c e d as it w a s c o n s u m e d , but there w a s a l w a y s d u c t i o n P I - 2 2 9 3 5 8 . On groundnut H. zea pupated 3 e x c e s s foliage in the cup. L a r v a e were w e i g h e d d a y s earlier o n Florigiant a n d N C - 2 (susceptible) w h e n they w e r e 11 d a y s old, a n d mortality t h a n o n N C - 6 (resistant). r e c o r d e d . Heliothis larvae did not survive on leaves of groundnut species from sections Ambinervosae, Laboratory Screening Wild Species Extranervosae a n d Erectoides. W h e n larvae w e r e fed groundnuts from the section Rhizomatosae, Field-grown Plants weight gain w a s low, a n d mortality a v e r a g e d 8 0 % . G r o u n d n u t s in t h e section Arachis, m o r e closely related to cultivated g r o u n d n u t s than s p e c i e s of Leaves were collected from selected field-grown other groups, caused moderate reduction in weight wild species to compare their relative resistance gain, a n d larval mortality a v e r a g e d 57.5%. Larvae w h e n H.zea did not h a v e a c h o i c e of oviposition fed leaves of cultivated groundnut did not differ substrates. Excised leaves were placed in plastic f r o m e a c h other in weight gain or mortality, but they bags a n d transported from the field to the labora• had only 20% mortality and their weights were two tory in a cooler filled with ice. to three times m o r e than the a v e r a g e weight of the Leaflets were placed in plastic jelly cups (4 x 4.5 larvae that survived for 11 d a y s on the wild s p e c i e s cm) and one 4-day-old larva was placed in each (Table 13). c u p . T h e c u p s were o b s e r v e d daily, a n d f o o d w a s

Greenhouse-grown Plants

Table 11. Antibiosis as a mechanism of resistance In Excised leaves from wild species were c o m p a r e d groundnut cv NC-6 to Heliothis zea, North Carolina, with cultivated groundnut for effect on H. zea d e v e l • U S A , 1 9 7 9 . o p m e n t a n d survival. L e a v e s were p l a c e d in plastic

Average wt of larvae (mg) c u p s (4 x 4.5 c m ) a n d a single 4 - d a y - o l d larva w a s C u l t i v a r Test 1a T e s t 2b p l a c e d in e a c h cup. T h e experiment w a s replicated six times a n d w h e n the larvae w e r e 10 d a y s old, N C - 6 1 9 . 2 1 0 . 4 they were weighed and mortality was recorded. N C - 2 5 3 . 4 3 4 . 7 Larvae did not survive on leaves of A. batizocoi F l o r i g i a n t 6 6 . 3 5 5 . 0 Krap. et G r e g . (Coll. G K P - 9 4 8 4 of s e c t i on Arachis) L S D ( 0 . 0 5 ) 2 0 . 8 1 4 . 3 or on A. sp. G K - 1 0 5 9 6 C of section Rhizomatosae. There was some larval mortality on all wild species a . Mean is an average for five 10-day-old but there w a s no mortality on N C - 2 or N C - 6 . Larvae l a r v a e . reared on the wild species w e i g h e d less t h a n those b . Mean is an average for eight 10-day-old reared on the N C - 2 susceptible standard (Table l a r v a e . 14).

Table 12. Effect of groundnut cultivar on Heliothis zea development, laboratory teat, North Carolina, U S A , 1 9 8 1 .

Average wt of D a y s t o D a t e o f C u l t i v a r 11-day-old larvae p u p a t i o n e m e r g e n c e ( m g )

N C - 6 1 0 , 0 2 9 . 2 2 A p r i l NC-6 x 3033 1 1 . 1 2 9 . 0 4 A p r i l N C - 2 3 3 . 2 2 5 . 5 3 1 M a r c h F l o r i g i a n t 3 6 . 5 2 5 . 8 3 1 M a r c h

L S D ( 0 . 0 5 ) 1 3 . 2 2 . 2 2.3a

a . D a y s

2 7 4 T a b l e 1 3 . L a b o r a t o r y e v a l u a t i o n o f H e l i o t h i s z e a f e e d i n g and survival on field-grown Arachis collections.

N o . o f A v e r a g e a n d r a n g e o f A v e r a g e a n d r a n g e o f S e c t i o n g e n o t y p e s l a r v a l w e i g h t g a i n m o r t a l i t y ( m g ) (%)

Arachis 8 6 8 5 7 . 7 ( 2 0 - 1 5 0 ) ( 4 0 - 8 0 ) Erectoides 6 0 1 0 0 Rhizomatosae 3 3 7 8 0 ( ( 0 - 6 0 ) ( 6 0 - 1 0 0 ) Ambinervosae 1 0 1 0 0 Extranervosae 1 0 1 0 0 Cultivated checks F l o r i g i a n t 1 0 0 2 0 N C - 2 1 3 0 2 0 N C - 6 1 1 0 2 0

T a b l e 1 4 . D i f f e r e n c e s among wild species of groundnut grown in the greenhouse on H e l i o t h i s z e a d e v e l o p m e n t , N o r t h C a r o l i n a , U S A .

A r a c h i s A v e r a g e w t o f A v e r a g e S p e c i e s C o l l e c t i o n S e c t i o n 1 0 - d a y - o l d l a r v a e m o r t a l i t y ( m g ) (%)

A. hypogaea N C - 2 Arachis 2 9 . 5 0 A. hypogaea N C - 6 Arachis 1 6 . 9 0 A. monticola K - 7 2 6 4 Arachis 1 1 . 7 1 6 . 7 A. s p G K P - 9 6 4 5 Rhizomatosae 4 . 9 5 0 . 0 A. s p M a n f r e d i # 5 Arachis 3 . 8 8 3 . 3 A. s p G K P - 9 6 4 9 Rhizomatosae 3 . 4 6 6 . 6 A. batizocoi G K P - 9 4 8 4 Arachis NR 1 0 0 A. s p G K - 1 0 5 9 6 C Rhizomatosae NR 1 0 0

L S D ( 0 . 0 5 ) 1 7 . 4

NR = not recorded.

Conclusion nomic importance in a pest-management approach. Defoliation among resistant groundnut There is evidence of moderate resistance to H. zea lines was usually below the damage threshold; among cultivated groundnuts. Resistance in NC- therefore insecticide applications would not be GP 343 and NC-Ac 342 is heritable. The wild spe• required for Heliothis control on resistant ground- cies of Arachis exhibited a high level of resistance nuts, and pesticide-induced mite outbreaks can be to H. zea, some approaching immunity. avoided. Antibiosis appears to be a major mechanism of resistance to H. zea in groundnut; however, ovipo- References sitional nonpreference has not been tested. BELAND, G.L., and HATCHETT, J.H. 1976. Expres• While the level of resistance to H. zea a m o n g sion of antibiosis to the bollworm in two soybean geno• cultivated peanuts is low to moderate, it is of eco • types. Journal of Ecoomic Entomology 69:557-560.

2 7 5 BRETT, C.H. 1958. Resistant corn to control corn earworm. North Carolina Research and Farming 16:6.

CAMPBELL, W.V. 1978. Effect of pesticide interactions on the two-spotted spider mite on peanuts. Peanut Science 5:83-86.

CAMPBELL, W.V., and WYNNE, J.C. 1979. Resist• ance of NC-6 peanut cultivar to Heliothis zea. P r o c e e d • ings, American Peanut Research and Education Societ y 11:63.

CAMPBELL, W.V., and WYNNE, J.C. 1980. R e s i s t • ance of groundnuts to insects and mites. Pages 149-1 5 7 in Proceedings, International Workshop on Groundnuts. ICRISAT, 13-17 Oct 1979, Patancheru, A.P., India.

CLARK, W.J., HARRIS, F.A., MAXWELL, F.G., and HARTWIG, E.E. 1972. Resistance of certain soybean cultivars to bean leaf beetle and bollworm. Journal o f Economic Entomology 65:1669-1672.

DOUGLAS, W.A. 1954. Effect of planting date on corn earworm damage to dent corn. Journal of Economic Ento • m o l o g y 4 7 : 1 1 5 8 .

DOUGLAS, W.A., and ECKHARDT, R.C. 1957. D e n t corn inbreds and hybrids resistant to the corn earwor m i n the south. U.S. Department of Agriculture, technica l b u l • letin 1160, Washington DC, USA. 13pp.

LEUCK, D.B., HAMMONS, R.O., MORGAN, L.W., and HARVEY, J.E. 1967. Insect preference for peanut varie• ties. Journal of Economic Entomology 60:1546-1549.

LUCKMAN, W.H. 1956. Observations on the European corn borer and the corn earworm infesting early season plantings of Country Gentleman sweet corn. Journal of Economic Entomology 49:877

LUKEFAHR, M.J., MARTIN, D.F., and MEYER, J.R. 1965. Plant resistance to five Lepidoptera attacking cot • ton. Journal of Economic Entomology 58:516-518.

MAXWELL, F.G., JENKINS, J.N., and PARROTT, W.L. 1972. Host plant resistance to insects. Advances in A g r o n o m y 2 4 : 1 8 7 - 2 6 5 .

McMILLIAN, W.W., and WISEMAN, B.R. 1972. H o s t plant resistance: A twentieth century look at the rel a t i o n • ship between Zea mays L. a n d Heliothis zea ( B o d d i e ) . Florida Agricultural Experimental Station monograph ser• ies 2, Fla, USA. 131 pp.

PAINTER, R.H. 1951. Insect resistance in crop plants. New York, USA: Macmillan. 520 pp.

STINNER, R.E., RABB, R.L., and BRADLEY, J.R. 1 9 7 6 . Natural factors operating in the population dynam• ics of Heliothis zea in North Carolina. Pages 622-642 in Proceedings. 15th International Congress of Entomolo g y , Washingon, DC, USA.

2 7 6 Screening Legumes for Resistance to Heliothis

D.J. Rogers*

Abstract

Resistance or differential susceptibility to Heliothis species—H. armigera, H. punctigera, H. virescens, and H. zea-has been demonstrated in Arachis hypogaea, Cajanus cajan, Cicer arietinum, Glycine max, Lablab purpureus, Medicago sativa, and Phaseolus vulgaris. Knowl• edge of Heliothis biology on the host and of the relationship of the pest infestation to host- plant phenology is essential to the development of realistic and effective methods of screen• ing for Heliothis resistance. In general, Heliothis infestation of legumes occurs during the flowering period, with larvae feeding on young leaves for a short time before completing development on the flowers and pods. Therefore techniques based on pod feeding are more appropriate, in most cases, than those based solely on leaf feeding. While germplasm col• lections and segregating populations are being screened for Heliothis resistance, knowledge of optional screening techniques would increase progress in the development of Heliothis- resistant legume cultivars.

The earliest published records of resistance or dif• has e x p a n d e d rapidly. T h e legumes in w h i c h host- ferential susceptibility to Heliothis within legume plant resistance to Heliothis has been reported are species were for chickpea (Cicer arietinum) a n d Arachis hypogaea (groundnut), Cajanus cajan hyacinth b e a n (Lablab purpureus) (Parsons et al (pigeonpea) Cicer arietinum (chickpea) Glycine 1938; Parsons and Marshall 1939). They reported max (soybean), Lablab purpureus (hyacinth bean), that H. armigera larvae bred on a purple-flowered Medicago sativa (lucerne), and Phaseolus vulgaris c h i c k p e a cultivar p r o d u c e d small p u p a e a n d adults ( c o m m o n bean). T h e Heliothis species for which with r e d u c e d fecundity, while those bred on a host-plant resistance in legumes is known are H. white-flowered cultivar produced normal-sized armigera (Hubner), H. punctigera (Wallengren), H. individuals with normal fecundity. They also noted virescens (F), and H. zea (Boddie). that three strains of hyacinth bean differed in the level of H. armigera oviposition during the preflowering period. No further cases of host-plant resist• General Principles of Screening a n c e to Heliothis in l e g u m e s a p p e a r e d in the literature until 1967 ( L e u c k et al. 1967). Since t h e n Plants for Resistance to Insects the literature on Heliothis resistance in l e g u m e s Reviews have been published by O r t m a n a n d

*Department of Primary Industries, Kingaroy, Queensland, Australia. Peters (1980), Dahms (1972), Kogan (1975), Guth-

International Crops Research Institute for the Semi- Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management 15-20 November 1981, Patancheru. A.P., India. 2 7 7 rie(1975), Farrell (1977), and Russell (1978) on the show adequate differences between susceptible general principles of screening plants for resist- a n d resistant genotypes. a n c e to insects. T h e s e publications highlight a number of features common to all screening for host-plant r e s i s t a n c e to insects. Insect Biotypes

Insect biotypes with the ability to infest previously Pest Biology resistant plant g e n o t y p e s have b e e n d e t e c t e d in s o m e insect pests of legumes. T h e r e has been no K n o w l e d g e of the biology of the pest a n d its rela• e v i d e n c e that any Heliothis s p e c i e s have d e v e - tionship to t h e p h e n o l o g y of the host plant is e s s e n • loped s u c h biotypes (Gallun a n d K h u s h 1980). tial before realistic screening tests for host-plant resistance c a n b e d e v e l o p e d . Information o n the distribution, feeding, a n d reproductive habits, a n d Biology of Heliothis Species on factors that affect the growth, survival, a n d fecundity of t h e pest are all important. S c r e e n i n g On legumes, the most important Heliothis species tests s h o u l d fall within the range of n o r m a l pest are H. armigera, H. punctigera, H. virescens, a n d H. behavior a n d activities on the host a n d should not zea. The biology of these species exhibits basic p r e c l u d e the expression of any a s p e c t of resist• similarities (Hardwick 1965; Turnipseed 1973; a n c e to the pest. K o g a n et al. 1978; Turner 1980). All four species are polyphagous, feeding on a wide range of culti• vated a n d uncultivated plant species. Assessment Methods On l e g u m e s , the Heliothis larvae feed on the leaves, g r o w i n g points, flowers, fruits, a n d seeds. Screening methods for resistance use either a W h e n periods of Heliothis activity occur during plant reaction or an insect response to quantify vegetative g r o w t h stages, significant a m o u n t s of host variation in resistance to t h e pest. D a h m s leaf f e e d i n g c a n occur. However, o n c e flowering (1972) identified 16 criteria that c o u l d be used to commences, feeding occurs preferentially on evaluate resistance in plants, involving both insect- reproductive plant parts. Heliothis species have a b a s e d a n d p l a n t - b a s e d a s s e s s m e n t t e c h n i q u e s . m a r k e d preference for oviposition on plants that In initial studies involving large numbers of are flowering (Parsons 1940; Cruz 1975; Johnson diverse plant lines, rating s c h e m e s that quantify 1975; Hillhouse a n d Pitre 1976). Hillhouse a n d Pitre b r o a d differences in plant d a m a g e or insect (1976) f o u n d that on s oy beans, this preference was numbers are adequate, although phenology differ• not as strong for H. virescens as H. zea. On soy• e n c e s a m o n g lines should be taken into a c c o u n t . beans, most Heliothis eggs are laid on leaves in the M o r e detailed a n d precise evaluations on levels upper two-thirds of the c r o p c a n o p y , with the a n d types of resistance are required for those lines youngest fully expanded trifoliolate leaf being the s h o w i n g s o m e resistance in initial tests. Evaluation most preferred oviposition site (Hillhouse a n d Pitre m e t h o d s must be a d e q u a t e to identify genetic 1976; Panda a n d Daugherty 1976). Turner (1974, plant-to-plant or line-to-line variation in resistance personal communication) found that most H. in heterogeneous populations. armigera eggs are laid on the fully expanded trifoli• olate leaves of flowering c o m m o n - b e a n plants.

Hatchett et al. (1976) o b s e r v e d that first- a n d Insect Infestation Methodology second-instar larvae feed on leaves before attack• ing s o y b e a n pods. I have o b s e r v e d a similar situa• T h e level of pest infestation required is o n e that tion with H. armigera on s o y b e a n s in Australia. maximizes discrimination between susceptible and Newly emerged H. armigera larvae f e e d on y o u n g resistant plants, rather t h a n simply a very severe soybean trifoliolate leaves before attacking the infestation. T o o heavy a n infestation m a y m a s k pods. Saxena (1978) records a similar sequence moderate, but still useful, levels of resistance a n d for H. armigera on p i g e o n p e a in India. McWilliams unnecessarily narrow the g e n e b a s e of the crop. a n d B e l a n d (1977) f o u n d that H. zea larvae deve- However, t o o light an infestation will i n c r e a s e t h e loped faster a n d h a d lower mortality on t h e upper- number of plants that escape attack and will not most e x p a n d i n g t h a n on the older trifoliolate leaves.

2 7 8 In addition, w h e n given a c h o i c e of leaves of differ• moderate levels of resistance to H. zea in North ent ages, H. zea larvae f e d preferentially on the Carolina breeding lines a n d in the cultivars Early youngest leaf. Where first-instar H. zea larvae were Bunch and NC-6, with laboratory tests indicating given a choice of leaves, flowers, and pods, feeding that antibiosis is the m e c h a n i s m of H. zea resist• w a s m o r e c o m m o n o n leaves a n d p o d s than o n a n c e in N C - 6 . This cultivar was originally d e v e • flowers (Bailey 1979). loped for resistance to the southern c o r n rootworm T h e usual s e q u e n c e followed by a Heliothis (Diabrotica undecimpunctata howardi) but subse• infestation on legumes appears to be for moths to quently w a s s h o w n to be resistant to thrips (Frankli- lay eggs on leaves in the upper part of the c r o p niella fusca) and potato leafhopper (Empoasca c a n o p y during the flowering period; the newly fabae) as well as H. zea. Current research in North h a t c h e d larvae f e e d on y o u n g trifoliolate leaves Carolina is directed towards c o m b i n i n g this multi• a n d flowers before co mp l e t i ng larval d e v e l o p m e n t ple pest resistance with resistance to s o m e on the pods. A n y s c r e e n i n g test for resistance to diseases. Heliothis species in legumes should take this s e q u e n c e into a c c o u n t . A less c o m m o n o c c u r • r e n c e is for larvae to feed on the leaves during the Cajanus cajan (Pigeonpea) vegetative growth stages. A screening test for leaf- feeding resistance should be c o n s i d e r e d separ• ICRISAT has an active program for screening ately f r o m a test to s c r e e n for resistance to the pest pigeonpea lines for resistance to H. armigera during the normal period of infestation, unless (Davies and Lateef 1978; Reed et al. 1980; ICRI• strong correlations exist b e t w e e n the two. SAT 1980). This program was initiated in 1975 in an attempt to identify reduced susceptibility to H. armigera a n d the podfly (Melanagromyza obtusa), Resistance to Heliothis in Particular and o n e of its objectives was to ensure that lines Legume Species generated by the ICRISAT plant breeders were not highly susceptible to H. armigera. References reporting aspects of resistance to Heli- A field-screening technique, using augmented othis species in legumes are s u m m a r i z e d in T a b l e natural H. armigera populations, has been deve• 1. S o m e of these are incidental (Parsons et al. loped. Initial evaluations in small unreplicated plots 1938; Parsons a n d Marshall 1939) or r e c o r d differ• have been c o n d u c t e d on almost 10 000 lines. e n c e s noted during the c o u r s e of other studies Promising lines were retested in replicated trials of (Bishop and Holtkamp 1980). Duangploy (1978) narrow maturity ranges, w h i c h include c h e c k c u l - reports the lack of a s o u r c e of resistance to Helio• tivars of known susceptibility. Spatial and temporal this in m u n g bean. For the other five l e g u m e spe- variations in pest attack result in high coefficients cies, the published data derive from conscious of variation. The use of balanced lattice-square attempts to identify and utilize resistance to Helio- designs in the a d v a n c e d testing stage gave useful this species. increases in efficiency. The percentage of pods d a m a g e d and the seed yield under unsprayed infested conditions were used to quantify the two Arachis hypogaea (Groundnut) aspects of resistance of interest to the ICRISAT t e a m . Leuck et al. (1967) documented significant varia• Lines with reduced susceptibility to H. armigera tion a m o n g 14 groundnut varieties in ratings of leaf attack have bee n identified, although n o n e appear defoliation in field-planted groundnuts. The defolia• to have immunity. Even the less susceptible lines tors were predominantly H. zea, with the velvet were severely attacked under heavy pest pressure. bea n caterpillar (Anticarsia gemmatilis), fall army- Lines vary widely in their ability to c o m p e n s a t e for w o r m (Spodoptera frugiperda) and red-necked H. armigera d a m a g e , a n d this c o m p e n s a t o r y ability peanut worm (Stegasta bosqueella) being present is an important selection criterion at ICRISAT. Con• in smaller numbers. Leuck et al. also found a signifi• siderable resistance to H. armigera has b e e n i d e n • cant negative correlation between the rating of leaf tified in Atylosia species, close wild relatives of d a m a g e by lepidopterous defoliators a n d a rating of pigeonpea, a n d attempts are being m a d e at ICRI• thrips d a m a g e . SAT to transfer this resistance to cultivated C a m p b e l l a n d W y n n e (1980) reported low t o pigeonpea.

2 7 9 Sinha et al. (1979) also report varietal differences Cruz (1975) provided the only record of differen- in susceptibility to H. armigera in pigeonpea. tial susceptibility to H. virescens in pigeonpea

Table 1. Literature of host-plant resistance to Helioth i s s p p I n l e g u m e s .

L e g u m e s p e c i e s H e l i o t h i s s p e c i e s R e f e r e n c e

Arachis hypogaea H. zea L e u c k e t a l . ( 1 9 6 7 ) (Groundnut) C a m p b e l l a n d W y n n e ( 1 9 8 0 )

Cajanus cajan H. armigera D a v i e s a n d L a t e e f ( 1 9 7 8 ) (Pigeonpea) S i n h a e t a l . ( 1 9 7 9 ) ICRISAT (1980) R e e d e t a l . ( 1 9 8 0 )

H. virescens Cruz (1975)

Cicer arietinum H. armigera P a r s o n s e t a l . ( 1 9 3 8 ) ( C h i c k p e a ) S i n g h a n d S h a r m a ( 1 9 7 0 ) S r i v a s t a v a e t a l . ( 1 9 7 5 ) D a v i e s a n d L a t e e f ( 1 9 7 8 ) ICRISAT (1980) R e e d e t a l . ( 1 9 8 0 )

Glycine max H. armigera T u a r t a n d R o s e ( 1 9 7 9 . p e r s o n a l c o m m u n i • ( S o y b e a n ) c a t i o n ) Rogers and Brier (unpublished data)

H. punctigera T u a r t a n d R o s e ( 1 9 7 9 . p e r s o n a l c o m m u n i • c a t i o n )

H. virescens H a t c h e t t e t a l . ( 1 9 7 6 ) T u r n i p s e e d a n d S u l l i v a n ( 1 9 7 6 ) H a t c h e t t e t a l . ( 1 9 7 9 )

H. zea C l a r k e t a l . ( 1 9 7 2 ) B e l a n d a n d H a t c h e t t ( 1 9 7 6 ) H a t c h e t t e t a l . ( 1 9 7 6 ) T u r n i p s e e d a n d S u l l i v a n ( 1 9 7 6 ) Tester (1977) Bell (1978) K e a e t a l . ( 1 9 7 8 ) H a t c h e t t e t a l . ( 1 9 7 9 ) D r e y e r e t a I . ( 1 9 7 9 ) S m i t h a n d B r i m ( 1 9 7 9 a , 1 9 7 9 b ) Joshi (1980)

Lablab purpureas H. armigera Parsons and Marshall (1939) ( H y a c i n t h b e a n )

Medicago sativa Heliothis s p p B i s h o p a n d H o l t k a m p ( 1 9 8 0 ) ( L u c e r n e )

Phaseolus vulgaris H. armigera Rogers (unpublished data) ( C o m m o n b e a n )

Vigna radiata Heliothis s p p Duangploy (1978) ( M u n g b e a n )

2 8 0 when he found significant differences in the Most of the research has been done on resist• number of H. virescens eggs laid on flowers and a n c e to H. zea a n d H. virescens. Twenty-four soy• pods and in the percentage of pods infested on 13 bean lines evaluated by Clark et al. (1972) for pigeonpea lines. resistance to bean leaf beetle (Cerotoma trifur- cata), striped blister beetle (Epicauta vittata), a n d bollworm (H. zea) included ten of the lines reported Cicer arietinum (Chickpea) by Van Duyn et al. (1971) as having resistance to the Mexican bean beetle (Epilachna varivestis). Parsons et al. (1938) recorded differences Lines PI-171451, PI-227687, and PI-229358 had between two chickpea cultivars in their suitability low pod-damage levels from H. zea. PI-227687 for H. armigera growth and development. Larvae received more eggs than other lines but had the feeding on a purple-flowered cultivar produced fewest damaged pods, suggesting antibiosis as the small pupae and adults with reduced fecundity, resistance mechanism. PI-171451 received fewer while larvae feeding on a white-flowered cultivar eggs than other lines. showed normal growth and development. Hatchett et al. (1976) evaluated the three resist• Singh and Sharma (1970) recorded variation in ant PI lines identified by Clark et al. (1972) and five susceptibility to damage by H. armigera, with t w o susceptible commercial cultivars in the laboratory lines being less damaged than three commercial for leaf-feeding resistance to H. zea a n d H. vires• cultivars. These two lines were also higher yielding, cens. All three PI lines produced higher larval mor• with good resistance to frost, wilt, and drought. tality, reduced larval weight gains, and increased Srivastava et al. (1975) studied 20 chickpea lines time to pupation in H. zea a n d H. virescens. Beland and found significant variation in the percentage of and Hatchett (1976) found that H. zea larval mortal• pods damaged. They found no correlation between ity occurred predominantly in the fifth to eighth seed yield and pod damage by H. armigera. instars and late in the intrastadial development in In recent years, ICRISAT has been screening PI-229358. The larvae feeding on the resistant PI- chickpea lines for resistance to H. armigera 229358 had at least one additional larval instar an d (Davies and Lateef 1978; Reed et al. 1980; ICRI• a longer development period than those feeding on SAT 1980). The approach to resistance screening susceptible cultivars. and the parameters used to quantify resistance are Turnipseed and Sullivan (1976) tabulated data the same as those used for pigeonpea. on multiple pest resistance—to H. zea, H. vires• Approximately 12 000 lines have been screened cens, E. varivestis, and Pseudoplusia includens— in the ICRISAT program, but no lines with immunity in breeding lines and indicated that where breeding have been identified. However, considerable and lines derived from PI-229358 were selected for consistent differences among chickpea lines in resistance to E. varivestis, some, but not all, lines susceptibility to H. armigera have been demon• were also resistant to H. virescens a n d H. zea. strated. As with pigeonpea, lines with substantial Hatchett et al. (1979) found that while PI-229358 compensatory ability have also been identified. was resistant to both H. zea and H. virescens, s o m e Selection of lines has been for reduced susceptibil• of the breeding lines derived from it were resistant ity to H. armigera and the ability to tolerate damage. to H. zea but not to H. virescens (see also Table 2, Individual plant selection in open-field conditions for another example of this). Hatchett et al. (1979) has not proved to be a useful technique. F2 popula• and Smith and Brim (1979a, 1979b) also examined tions derived from crosses using the less suscepti• selection for multiple pest resistance in crosses ble cultivars have been screened for resistance. between resistant PI lines and susceptible com• Selection within existing cultivars for reduced sus • mercial cultivars. Data from all four papers (Turnip- ceptibility to H. armigera has also been seed and Sullivan 1976; Hatchett et al. 1979; Smith investigated. and Brim 1979a, 1979b) indicate that while it is possible to recover lines with resistance to more than one pest, direct selection for resistance to o n e Glycine max (Soybean) pest species does not necessarily result in indirect selection for resistance to other pests.

As indicated in Table 1, host-plant resistance to H. In laboratory studies, ED 73-541 had substantial armigera, H. punctigera, H. virescens, and H. zea levels of resistance to H. zea a n d H. virescens in has been reported in soybeans. the USA (Turnipseed and Sullivan 1976) but is

2 8 1 Table 2. Comparative development of Heliothis armig e r a , H. virescens, a n d H . z e a on four soybean lines.a

H. armigeraa H. virescensb H. zeac L a r v a l w e i g h t L a r v a l w e i g h t Larval weight Soybean line 1 0 d a y s 1 3 d a y s 1 4 d a y s

D a v i s 4 7 8 . 2 a 2 9 7 . 9 a 3 7 7 . 8 a E D 7 3 - 1 7 3 4 9 1 . 1 a 2 4 3 . 2 b 3 4 0 . 7 a E D 7 3 - 5 4 1 4 7 4 . 2 a 1 5 9 . 6 d 2 0 7 . 8 b E D 7 3 - 3 7 1 3 3 8 . 1 b 1 8 6 . 7 c 1 9 2 . 1 b

a . Means in each column followed by the same letter are not significantly different at the 5%

l e v e l .

b . Data from laboratory experiment conducted by H.B. Br ier and D.J. Rogers, 1981.

c . Data from Turnipseed and Sullivan 1976.

susceptible to H. armigera in Australia (Brier and larvae that fail to survive. This suggestion is c o m • Rogers, u n p u b l i s h e d data). T h e s e c a s e s indicate patible with the findings of B e l a n d a n d Hatchett that indirect selection for resistance to a Heliothis (1976) on the s y m p t o m s of Heliothis larval d e a t h on s p e c i e s m a y be ineffective. In addition, it c a n n o t be the resistant lines. Dreyer et al. (1979) have iso• a s s u m e d that a breeding line resistant to o n e Helio• lated pinitol (3-0-methyl-chiro-inositol) from soy• this species will be resistant to other species of b e a n leaves. Pinitol c a u s e d a 5 0 % reduction in Heliothis. These studies indicate that multiple pest- weight gain of H. zea larvae w h e n present at 0.7% in resistant parent lines s u c h as PI-227687 a n d P l - a synthetic diet. In both cv Davis a n d PI-229358, 2 2 9 3 5 8 c o n t a i n a n u m b e r of independently the yield of crystalline pinitol w a s about 1 % of dry inherited c a u s e s of resistance to insects. weight (Dreyer et al. 1979); however, as there is a Josh i (1 9 8 0 ) e x a m i n e d the effect of planting substantial difference in the response of H. zea to dates a n d cultivars on s o y b e a n p o d d a m a g e by H, these two lines, it appears unlikely that pinitol is the zea a n d f o u n d that the insect-resistant breeding c a u s e of resistance to Heliothis in the line PI- line ED 73-371 h a d the highest a m o u n t of active H. 2 2 9 3 5 8 . zea infestation, but low levels of p o d d a m a g e . This K e a et al. (1978) a n d Bell (1978) studied the c o n t r a s t e d with the findings of Kea et al. (1978) that effect of insect-resistant s o y b e a n lines on the c o n • ED 73-371 had significantly lower natural H. zea trol of H. zea by other methods. In laboratory s t u • populations than cv Bragg. dies, H. zea larvae fed leaves of the line ED 73-371 Two studies on possible chemical bases of w e r e m o r e susceptible to m e t h o m y l a n d Bacillus insect resistance in t h e PI lines have b e e n p u b • thuringiensis, c o m p a r e d with larvae fed on cv lished (Tester 1977; Dreyer et al. 1979). Tester B r a g g ( K e a et al 1978). In the field, higher levels of (1977), examining total nitrogen, carbohydrates, H. zea control were obtained with methyl-parathion a n d sterols, f o u n d that susceptible varieties a n d B. thuringiensis on ED 73-371 t h a n on cv a c c u m u l a t e d m o r e total nitrogen a n d at a faster Bragg, at the s a m e pesticide application rates. Bell rate t h a n the resistant lines. At p o d filling, resistant (1978) examined the interactions between the lines h a d 3 3 % m o r e soluble c a r b o h y d r a t e . T h e res• pathogens S. thuringiensis a n d Nomuraea rileyi istant lines accumulated sterols faster than sus• a n d insect-resistant a n d susceptible soybeans . H e ceptible cultivars and, by p o d filling, c o n t a i n e d 20 to f o u n d a c o m b i n a t i o n of t h e resistant line P I - 2 2 7 6 8 7 5 0 % m o r e t h a n susceptible cultivars. Tester (1977) and either of the pathogens caused higher H. zea s u g g e s t e d that insect resistance in t h e PI lines m a y larval mortality in a shorter period of time t h a n result f r o m t h e p r e s e n c e of plant sterols with j u v e • single factors acting alone. nile h o r m o n e activity. He indicated that e x p o s u r e of R e s e a r c h on resistance to H. armigera a n d H. later instar larvae to juvenile h o r m o n e a n a l o g u e s punctigera have been c o n d u c t e d by Tuart a n d would prevent n o r m a l d e v e l o p m e n t to the adult Rose (personal communication 1979) and Brier stage a n d result in t h e formation of s u p e r n u m e r a r y a n d Rogers (unpublished data). Tuart a n d Rose, in

2 8 2 a laboratory feeding study using three PI lines a n d with the main emphasi s on w h i t e - s e e d e d dry cv Bragg, found higher larval mortality, slower lar• beans. S o m e work has also been d o n e on H. armig• val growth, and an extended larval development era resistance in snap-bean cultivars. period for both H. armigera a n d H. punctigera. P l - Bean lines were s c r e e n e d in the field, using a u g • 2 2 7 6 8 7 w a s the line most resistant to H. armigera. m e n t e d natural H. armigera populations. Initial eva• M o r e detailed laboratory feeding studies have luations were in small replicated plots laid out in been conducted by H.B. Brier and myself on H. lattice-square designs. Promising lines were armigera, using Australian commercial varieties, retested in larger plots with more replications a n d the three resistant PI lines a n d a number of b r e e d • laid out in lattice-square or rectangular-lattice ing lines supplied by M.J. Sullivan, C l e m s o n Univer• experimental designs. In the initial screening sity, South Carolina, USA. We have not found the experiments, relative infestation levels were quan• high levels of larval mortality documented by Tuart tified using the percentage of pods a n d seeds d a m • and Rose (personal communication, 1979), or by aged. A sample of 50 pods per plot w a s found to be A m e r i c a n workers for H. zea a n d H. virescens. adequate in most situations. H. armigera larval However, the three PI lines a n d s o m e of the breed• population levels were also recorded in evaluations ing lines have c a u s e d prolonged larval d e v e l o p • of promising lines, in addition to the two plant- ment periods and smaller pupae. Our studies damage parameters. Where there was variation support the finding of Tuart and Rose (1979) that of a m o n g lines in days to flowering, serial plantings of t h e three PI lines, PI-227687 is t h e most resistant to a photoperiod-insensitive, early-flowering sus• H. armigera. Of the breeding lines, ED 73-371 had ceptible cultivar were made, to provide a basis for the highest level of resistance, affecting H. armig• comparisons a m o n g the lines under test. era growth and development to the same extent as Of 600 lines evaluated, no lines were found with PI-227687. immunity to attack. However, susbstantial and con• sistent differences in levels of H. armigera infesta• Lablab purpureas (Hyacinth Bean) t i o n a n d p o d a n d s e e d d a m a g e w e r e demonstrated. Some lines were considerably m o r e T h e only record of variation in susceptibility to Heli- susceptible to H. armigera infestation than others othis species in L. purpureus is a brief reference by (Table 3). In addition to evaluating lines from g e r m - Parsons a n d Mitchell (1939). T h e y noted that plasm collections, lines bred by E.C. Gallagher in a extensive oviposition o c c u r r e d on a Rhodesian dry-bean breeding program have b e e n evaluated strain of L. purpureus before flowering, while on two for relative susceptibility. Some experimental work other varieties, oviposition began only after flower• has been done on bean-pod fiber content a n d H. ing c o m m e n c e d . T h e R h o d e s i a n strain emitted a armigera resistance status. T h e feasibility of strong scent e v e n w h e n y o u n g , while the other t w o single-plant selection for H. armigera pod-feeding strains did not. resistance under field conditions has been investi• gated. In 1980, laboratory studies were initiated to Medicago sativa (Lucerne) obtain data on the m e c h a n i s m s of resistance. Both leaf- a n d p o d - f e e d i n g s t u d i e s h a v e b e e n Bishop a n d H o l t k a m p (1980) d o c u m e n t e d signifi• c o n d u c t e d . cant differences in susceptibility to Heliothis attack among the lucerne cultivars Condura 73, CUF-101, Vigna radiata (Mung Bean) a n d Hunter River. Hunter River had significantly more, and CUF-101 had significantly fewer, Duangploy (1978) listed Heliothis s p e c i e s as infested s t e m s than C o n d u r a 73. As the Heliothis important pests of mung bean in Thailand a n d larvae developed fully on all three varieties, Bishop states that severe d a m a g e c a n occur. He indicates and Holtkamp (1980) suggested that ovipositional that no source of resistance to Heliothis species nonpreference may be the cause of the has been reported in m u n g bean. differences.

Phaseolus vulgaris (Common Bean) General Comments

Since 1977, l have c o n d u c t e d a r e s e a r c h p r o g r a m In groundnut, lucerne, and soybeans, the reported on resistance to H. armigera in the c o m m o n b e a n , c a s e s of resistance to Heliothis species are in plant

2 8 3 What constitutes an appropriate assessment Table 3. Resistance to Heliothis a r m i g e r a I n m e t h o d of s c r e e n i n g for Heliothis resistance is Phaseolus vulgaris, as Indicated by percent pod important. In situations w h e r e Heliothis leaf feeding d a m a g e . is of most c o n c e r n , m e t h o d s that quantify the a m o u n t of leaf feeding or the size of pest popula• Podsa d a m a g e d I d e n t i t y by H. armigera tions f e e d i n g on t h e leaves w o u l d be appropriate. (%) W h e r e p o d feeding by Heliothis is t h e reason for its pest status, a s s e s s m e n t methods b a s e d solely on Brown Swedish 5 1 . 3 m e a s u r e m e n t s of leaf feeding do not appear to be R o y a l W i n d s o r 3 8 . 7 entirely satisfactory unless strong correlations Brown Beauty 3 8 . 0 exist b e t w e e n the two. Hatchett et al. (1976) r e c o g • T e x c o c o 4 3 6 . 7 nized this problem. Parameters that have b e e n Dwarf Horticultural 3 6 . 7 used successfully to quantify pod-damage levels Orbit 131373 3 3 . 3 are: the p e r c e n t a g e of d a m a g e d p o d s (Singh a n d Standard Pink No. 38 2 8 . 0 S h a r m a 1970; Srivastava et al. 1975; ICRISAT Pintous No. 14 2 6 . 0 1980; Rogers unpublished data), the n u m b e r of Light Red Kidney 2 6 . 0 d a m a g e d pods (Clark et al 1972; Joshi 1980), a n d a P R - 6 2 3 . 3 Negro 325 (P-438)c 2 3 . 3 rating of p o d d a m a g e (Joshi 1980). In other publi• Jamapa (P-460) 2 2 . 0 cations, only leaf-damage ratings are given (Hat• Tara (P-567) 2 2 . 0 chett et al. 1976, 1979; Smith a n d Brim 1 9 7 9 a , P R - 1 6 2 2 . 0 1979b). PI-208769 (P-231) 2 1 . 3 T h e effect of phenology of lines on s c r e e n i n g for P I - 1 5 0 4 1 4 1 8 . 7 p o d - f e e d i n g resistance to Heliothis has b e e n rec• PI-309796 (P-303) 1 8 . 7 ognized, a n d experimental m e t h o d s d e v i s e d to cir• Negro 321 (P-437) 1 8 . 0 c u m v e n t t h e problem. In c h i c k p e a a n d pigeonpea PI-310814 (P-8) 1 7 . 3 lines are divided into narrow maturity-range groups Antioquia 23 1 5 . 3 Veranic 2 (P-538) 1 5 . 3 (ICRISAT 1980), while in c o m m o n bean, serial Negro 324 (P-436) 1 4 . 7 plantings of a susceptible cultivar are used (Rog• S m a l l W h i t e F M 5 2 1 4 . 0 ers, unpublished data). In photoperiod-sensitive PI-207262 (P-684) 1 4 . 0 crops, s u c h as soybeans, an additional a p p r o a c h in P i - 1 6 5 4 2 6 1 2 . 7 m a s s - s c r e e n i n g p r o g r a m s m a y b e t o use maturity L S D - ( 0 . 0 5 ) 1 2 . 6 isolines of a susceptible cultivar to allow compari• C V (%) 3 4 . 2 s o n of lines with different maturities. In s o m e studies of Heliothis resistance in a . All lines commenced flowering 7-10 legumes, insects from laboratory colonies have March 1979. b e e n u s e d in laboratory a n d field experiments b . Susceptible check cultivar. (Clark et at. 1972; B e l a n d a n d Hatchett 1976; Hat• c . All P-numbers in parentheses are CIAT chett et al. 1 9 7 6 , 1 9 7 9 ; Bell 1978; K e a et al. 1978; Promising Line numbers (Source: Smith a n d Brim 1979a). However, the d o c u m e n t e d A n o n y m o u s 1 9 7 8 ) . differences in behavior and population genetic structure b e t w e e n Heliothis field populations and laboratory colonies (Raulston 1975; Sluss et al. lines a l r e a d y k n o w n to be resistant to other pests 1978) suggest that s o m e caution s h o u l d be exer• ( C a m p b e l l a n d W y n n e 1980; B i s h o p a n d H o l t k a m p cised when using laboratory-bred Heliothis for e v a • 1980; C l a r k et al. 1972). In e a c h c a s e , r e s i s t a n c e to luation of l e g u m e s for Heliothis resistance. t h e first pest w a s identified in a g e r m p l a s m s c r e e n • Evaluation of l e g u m e s for Heliothis resistance ing p r o g r a m in w h i c h most lines w e r e d i s c a r d e d has usually involved laboratory feeding studies. b e c a u s e of susceptibility to t h e pest. It is possible While in g e n e r a l there a p p e a r s to be a c l o s e cor• that additional useful sources of resistance to Heli• r e s p o n d e n c e b e t w e e n t h e results of field a n d othis m a y h a v e b e e n o v e r l o o k e d b e c a u s e they laboratory tests, this does not always occur. For w e r e s u s c e p t i b l e to the other pest species. S c r e e n • e x a m p l e , the ft s o y b e a n line IR-5 w a s f o u n d to ing the original germplasm specifically for resist• p r o d u c e significant effects on H. zea g r o w t h a n d a n c e to Heliothis m a y be worthwhile. d e v e l o p m e n t in the laboratory, but most of the

2 8 4 inbred lines derived from IR-5 were f o u n d suscepti• cies is a rapidly expanding area of l e g u m e e n t o • ble to H. zea in the field by Hatchett et al. (1979). mology. Since its beginnings in the late 1960s a n d They suggest that in segregating plant populations, early 1970s, rapid progress has b e e n m a d e in the laboratory bioassay tests m a y give only a partial identification of Heliothis-resistant lines. While pro• indication of field response. This particular exam• gress has not been as rapid in incorporation of ple suggests that d e p e n d e n c e on laboratory tests these resistances into c o m m e r c i a l l y a c c e p t a b l e alone is inadequate in evaluating l e g u m e s for res• cultivars, considerable advances have been made. istance to Heliothis and that field experimentation Increased knowledge of optimal Heliothis- should always be an important part of any s u c h resistance screening methods for segregating program. Most laboratory bioassays have involved populations would increase progress substantially. leaf feeding; however, the biology of Heliothis on T h e work that has been done on the influence of legumes suggests that a more realistic test would Heliothis-resistant cultivars on other control tech• be o n e that involves larval leaf feeding for the first niques is extremely valuable. S u c h knowledge will few days, followed by pod feeding until pupation. provide the basis for the incorporation of Heliothis- Heliothis resistance in legumes is not immunity; resistant cultivars into integrated pest manage- its evaluation therefore c a n n o t be based merely on ment systems for legume crops. the p r e s e n c e or a b s e n c e of insects or d a m a g e . It requires precise quantification of the relative a m o u n t of infestation or d a m a g e . W o r k on chick- References pea a n d c o m m o n bean (ICRISAT 1980; Rogers, ANONYMOUS. 1978. Catalogue of promising bean unpublished data) indicates that spatial a n d t e m - materials. Centra Internacional de Agricultura Trop i c a l e , poral variation in pest attack make it very difficult to Cali, Colombia. 90 pp. detect real relative differences in Heliothis d a m a g e or infestation of pods on single plants in the field. BAILEY, J.C. 1979. Preference of day-old bollworms (Lepidoptera; Noctuidae) for selected parts of soyb e a n This s u g g e s ts that selection for resistance in F2 plant. Journal of the Kansas Entomological Society 52(3): populations in the field w o u l d not be worthwhile, 621 - 6 2 2 . though screening of F2 populations m a y be possible in a m o r e controlled situation, s u c h as in a BASS, M.H., and ARANT, F.S. 1973. Insect pests. g r e e n h o u s e . Attempts are being m a d e at ICRISAT Pages 383-428 in Peanuts—culture and uses. American to s c r e e n F2 c h i c k p e a populations (Reed et al. Peanut Research and Education Association. 684 pp.

1980). A number of workers have evaluated F3 to F6 BELAND, G.L., and HATCHETT, J.H. 1976. E x p r e s • lines in t h e field a n d laboratory a n d f o u n d signifi- sion of antibiosis to the bollworm in two soybean g e n o • cant differences among breeding lines. Some of types. Journal of Economic Entomology 69: 557-560. these breeding lines w e r e as resistant to Heliothis BELL, J.V. 1978. Development and mortality in boll- as the resistant parents (Beland and Hatchett worms fed resistant and susceptible soybean cultivars 1976; Turnipseed and Sullivan 1976; Hatchett et al. treated with Nomuraea rileyi or Bacillus thuringiensis. 1979; Smith and Brim 1979a, 1979b). Adequate Journal of the Georgia Entomological Society 13: 50 - 5 5 . field a s s e s s m e n t s a n d laboratory bioassay tests for BISHOP, A.L., and HOLTKAMP, R.H. 1980. Heliothis pod-feeding resistance to Heliothis require reaso• species on three varieties of lucerne infested with b l u e - nable amounts of plant material. This can be green aphid Acyrthosiphon kondoi Shinji. General and obtained w h e n using F3 and later lines, but not with Applied Entomology 12: 10-12. F2 populations. W h e r e leaf-feeding resistance to CAMPBELL, W.V., and WYNNE, J.C. 1980. Resistance Heliothis is required, it is possible that selection of groundnuts to insects and mites. Pages 149-157 in within F2 populations m a y present fewer problems. Proceedings, International Workshop on Groundnuts, 1 3 - However, in general, it appears that in a Heliothis 17 Oct 1980, ICRISAT, Patancheru, A.P., India. 324 p p . resistance plant-breeding program, selection on the p e r f o r m a n c e of F3 a n d later lines, in field a n d CLARK, W.J., HARRIS, F.A., MAXWELL, F.G., and laboratory tests, m a y be a better a p p r o a c h than HARTWIG, E.E. 1972. Resistance of certain soybean cultivars to bean leaf beetle, striped blister beet l e a n d selection on a single-plant basis in F2 populations. bollworm. Journal of Economic Entomology 65: 1669- 1 6 7 2 .

Conclusion CRUZ, C. 1975. Observations on pod borer oviposition and infestation of pigeonpea varieties. Journal of t h e A g r i • Breeding cultivars for resistance to Heliothis s p e - cultural University of Puerto Rico 59: 63-68.

2 8 5 DAHMS, R.G. 1972. Techniques in the evaluation and KEA, W.C., TURNIPSEED, S.G., and CARNER, G.R. development of host-plant resistance. Journal of Env i r o n • 1 9 7 8 . Influence of resistant soybeans on the susceptibil • mental Quality 1: 254-259. ity of lepidopterous pests to insecticides. Journal of E c o • nomic Entomology 71: 58-60. DAVIES, J.C., and LATEEF, S.S. 1978. Recent trends in grain legume pest research in India. Pages 25-31 in KOGAN, M. 1975. Plant resistance in pest manage• Pests of grain legumes; ecology and control, eds. S.R. ment. Pages 103-146 i n Introduction to insect pest man• Singh, M.H. van Emden, and T.M. Taylor. London, UK: agement, eds. R.L. Metcalf and W.Luckmann, New York, Academic Press. USA: John Wiley. KOGAN, J., SELL, D.K., STINNER, R.E., BRADLEY, DREYER, D.L., BINDER, R.G., CHAN, B.G., WAISS, J.R., and KOGAN, M. 1975. The literature of arthropods A.C., HARTWIG, E.E., and BELAND, G.L. 1979. P i n- associated with soybean. V. A bibliography of Heliothis itol, a larval growth inhibitor for Heliolhis zea in soybeans. zea (Boddie) and H. virescens (F.) (Lepidoptera: Noctui- Experientia 35:1182-1183. dae). University of Illinois, INTSOY Series 17, Urba n a , III, DUANGPLOY, S. 1978. Breeding mung bean for Thai• USA. 242 pp. land conditions. Pages 228-229 in Proceedings, First International Mungbean Symposium, ed. R. Cowell. Asi a n LEUCK, D.B., HAMMONS, R.O., MORGAN, L.W., and Vegetable Research and Development Centre, Taiwan. HARVEY, J.E. 1967. Insect preference for peanut varie• 2 6 3 p p . ties. Journal of Economic Entomology 60: 1546-1549.

McWILLIAMS, J.M., and BELAND, G.L. 1977. B o l l - FARRELL, J.A.K. 1977. Plant resistance to insects and worm: effect of soybean leaf age and pod maturity o n the selection of resistant lines. New Zealand Entomo l o g i s t development in the laboratory. Annals of the Entomo l o g i • 6: 244-261. cal Society of America 70: 214-216. GALLUN, R.L., and KHUSH, G.S. 1980. Genetic fac• NIELSON, M.W., and LEHMAN, W.F. 1980. B r e e d i n g tors affecting expression and stability of resistan c e . approaches in alfalfa. Pages 277-312 in Breeding plants Pages 63-86 in Breeding plants resistant to insects, eds. resistant to insects, eds. F.S. Maxwell and P.R. Jen n i n g s . F.S. Maxwell and P.R. Jennings. New York, USA: John New York, USA: John Wiley. 683 pp. Wiley. 683 pp.

ORTMAN, E.E., and PETERS, D.C. 1980. Introduction. GUTHRIE, W.D. 1975. Entomological problems P a g e s 3 - 1 4 in Breeding plants resistant to insects, eds. involved in developing host-plant resistance progra m s . F.S. Maxwell and P.R. Jennings. New York, USA: John Iowa State Journal of Research 49: 519-525. Wiley. 683 pp. HARDWICK, D.F. 1965. The corn earworm complex. PANDA, N., and DAUGHERTY, D.M. 1976. O v i p o s i • Memoirs, Entomological Society of Canada No. 40. tional p r e f e r e n c e of Heliothis zea (Hubn.) on glabrous and Ottawa, Canada. 248 pp. dense soybean genotypes. Madras Agricultural Journa l HATCHETT, J.H., BELAND, G.L., and HARTWIG, 63: 227-230. E.E. 1 9 7 6 . Leaf-feeding resistance to bollworm and PARSONS, F.S. 1940. Investigations on the cotton boll- tobacco budworm in three soybean plant introduction s . w o r m . Heliothis armigera Hubn. III. Relationships Crop Science 16: 277-280. between oviposition and the flowering curves of foo d - HATCHETT, J.H., BELAND, G.L., and KILEN, T.C. plants. Bulletin of Entomological Research 31:147-17 7 . 1 9 7 9 . Identification of multiple insect resistant soybea n PARSONS, F.S., and MARSHALL, J. 1939. P a g e s 2 8 - lines. Crop Science 19: 557-559. 35 in Progress reports from experiment stations, season HILLHOUSE, T.L., and PITRE, H.N. 1976. Oviposition 1937-38. Empire Cotton Growing Corporation, London by Heliothis on soybeans and cotton. Journal of Eco• (original article not seen. Abstract in Review of App l i e d nomic Entomology 69:144-146. Entomology 27: 4879).

ICRISAT. 1980. Pigeonpea entomology. Pages 98-103 PARSONS, F.S., HUTCHINSON, H., and MARSHALL, in ICRISAT annual report, 1978-79. Patancheru, A.P., J . 1 9 3 8 . Pages 26-32 i n Progress reports from experi• India: ICRISAT. ment stations, season 1936-37, Empire Cotton Growin g Corporation, London. (Original article not seen. Abs t r a c t JOHNSON, M.W., STINNER, R.E., and RABB, R.L. in Review of Applied Entomology 26:3644). 1 9 7 5 . Ovipositional response of Heliothis zea (Boddie) to its major hosts in North Carolina. Environmental En t o m o l • RAULSTON, J.R. 1975. Tobacco budworm: Observa• ogy 4. 291-297. tions on the laboratory adaptation of a wild strain. A n n a l s of the Entomological Society of America 68: 139-142 . JOSHI, J.M. 1980. Effect of planting dates and soybean cultivars on pod damage by corn earworm. Crop Scien c e REED, W., SESHU REDDY, K.V., LATEEF, S.S., 2 0 : 5 9 - 6 3 . AMIN, P.W., and DAVIES, J.C. 1980. The contribution of

2 8 6 ICRISAT to studies on plant resistance to insect attack. VAN DUYN, J.W., TURNIPSEED, S.G., and MAX• Presented at the Scientific Working Group Meeting o n WELL, J.D. 1971. Resistance in soybeans to the Mexi• Use of Naturally Occurring Plant Products in Pest a n d can bean beetle. I. Sources of resistance. Crop Sci e n c e Disease Control, May 1980, Nairobi, Kenya. 14 pp. 11:572-573. (Mimeographed.)

RUSSELL, G.E. 1978. Plant breeding for pest and dis• ease resistance. London, UK: Butterworth's. 485 pp.

SAXENA, H.P. 1978. Pests of grain legumes and their control in India. Pages 15-23 in Pests of grain legumes: ecology and control, eds. S.R. Singh, H.F. van Emde n . a n d T. Ajibola Taylor. London, UK: Academic Press.

SINGH, H., and SHARMA, S.S. 1970. Relative suscep• tibility of some important varieties of gram to Heliothis armigera Hubner. Indian Journal of Entomology 32:170- 1 7 1 .

SINHA, M.M., YADAV, R.P., and KUMAR, A. 1 9 7 9 . Multidirectional approach for pest-management in a r h ar (Cajanus cajan) in Bihar. Pesticides (Bombay) 13: 1 4 - 1 6 .

SLUSS, T.P., SLUSS, E.S., GRAHAM, H.M., and DUBOIS, M. 1978. Allozyme differences between Helio• this virescens a n d H. zea Annals of the Entomological Society of America 71: 191-195.

SMITH, C.M., and BRIM, C.A. 1979a. Field and labora• tory evaluations of soybean lines for resistance to c o r n earworm leaf feeding. Journal of Economic Entomology 72: 7 8 - 8 0 .

SMITH, C.M., and BRIM, C.A. 1979b. Resistance to Mexican bean beetle and corn earworm in soybean geno • types derived from PI-227687. Crop Science 19:313-31 4 .

SRIVASTAVA, A.S., SRIVASTAVA, K.M., and SINGH, L . N . 1975. Studies on relative resistance or susceptibility of gram varieties to gram pod borer, Heliothis armigera Hubner. Labdev Journal of Science and Technology 13B: 2 6 4 - 2 6 5 .

TESTER, CF. 1977. Constituents of soybean cultivars differing in insect resistance. Phytochemistry 16: 1 8 9 9 - 1 9 0 1 .

TURNER, J.W. 1980. Insect pests of peanuts in south• ern Queensland. Queensland Agricultural Journal 106: 1 7 2 - 1 7 6 .

TURNER, J.W., and TITMARSH, I. 1979. When is a soybean 'pest' a pest? Queensland Agricultural Jour n a l 105:355-362.

TURNIPSEED, S.G. 1973. Insects. Pages 545-572 i n Soybeans: improvement, production and uses, ed. BE. Caldwell. American Society of Agronomy Monograph 16, Madison, Wis, USA. 681 pp.

TURNIPSEED, S.G., and SULLIVAN, M.J. 1976. Plant resistance in soybean insect management. Pages 549- 5 6 0 in World soybean research, ed. L.D. Hill. Danville, III, USA: Interstate. 1073 pp.

2 8 7 Discussion — Session 5

In the discussion following this session, many such as the brown plant hopper. Fortunately, the details in the papers were questioned; the points of development of biotypes in Lepidoptera in general interest that emerged are summarized response to resistant crops is virtually unknown. here. There is an obvious need to check carefully the Screening for plant resistance should be com• mechanism of resistance to ensure that this does prehensive, probably including laboratory, green• not reduce the quality of a food or feed crop. house, and field-testing. The field testing should be In any crop, the level of resistance that will be of done both under natural infestation, to determine practical use will depend upon many factors, nonpreference for oviposition, and under artificial including the economic threshold for the pest and infestation to minimize the escape problem. Eva• the probable pest populations that the crop is likely luation systems need to be refined to allow the to face. There is a possibility that low levels of identification of small differences in susceptibility. resistance in the crop may act synergistically with Evaluations must be made over several sowing other pest-management elements. For example, dates and locations. For most successful screen• larvae feeding on resistant plants may be more ing programs, laboratory-rearing facilities for mas s susceptible to pesticide use. However, it is also rearing the pests, preferably on synthetic diets, a n d possible that resistant plants may have an adverse a methodology for the release of these pests on the effect upon the natural enemy complex. Also the materials to be screened, may be essential. How• incorporation of resistance in a plant to one pest ever, some screening programs have been suc• may change the susceptibility of that plant to other cessful using only natural field infestations. insects in the pest complex. Laboratory-bred test insects should be continually It was stressed that new high-yielding cultivars monitored to ensure that they do not differ mate• should be no more susceptible than those that are rially from the insects in the wild. Although at CI M- to be replaced. Morphological characters are the MYT no adverse effects were observed after 18 easiest to manage from the plant-breeding stand• generations of H. zea were reared on synthetic diet, point and should be given special emphasis in care is taken to introduce fresh insects from the screening programs. Multigenic resistance is most wild at frequent intervals. desirable, for it has broader utility and has generally For laboratory testing a knowledge of the feeding proved to be most stable. activity and of the plant parts used as food is ess e n • Wild species of plants may provide a valuable tial. For example, gossypol content was assumed reservoir of insect-resistance genes and are to be an important factor in the resistance of cotton expected to be of increasing utility in plant breeding to Heliothis, but careful study showed that Heliothis programs. The possibility of using genetic engi• larvae when feeding simply avoid the glands con• neering should be studied, and it is essential that taining gossypol. In the case of phloem feeders entomologists make full use of new developments. such as jassids, analysis of phloem content rather than of whole leaves is required when chemicals involved in resistance/susceptibility are investigated. The antibiosis mechanism of resistance would appear to be the most useful, for nonpreference can break down when insects do not have a choice, particularly when a resistant cultivar is grown over a wide area. It was pointed out, however, that for polyphagous pests such as Heliothis, nonpref• erence may hold for a long period and the develop• ment of biotypes of the pest is likely to be much slower in such insects than in more specific pests

2 8 8 Session 6

Novel Methods of Heliothis Management

Chairman: M. Jacobson Rapporteurs: H.C. Sharma Cochairman: H. Rembold C.S. Pawar

The Present Status and Potential for Novel Uses of Pheromone to Control Heliothis

A.N. Sparks, J.R. Raulston, J.E. Carpenter, and P.D. Lingren*

Abstract

Some 20 years after research was initiated on Heliothis zea (Boddie) and Heliothis virescens (F.) pheromones, they were identified in 1979. Since then, laboratory and field tests have been conducted to explore potential uses of these pheromones to monitor andlor disrupt mating ot Heliothis spp. populations. Pheromone traps have been designed and those measured have catch efficiencies in the 5 to 60% range, but the relationship of trap catch to actual popula• tion density remains unknown. Several experiments, limited to large-cage of small-field plots, have shown that H e l i o t h i s pheromone and/or mimics have measurable effects on H. zea or H. virescens, but none have shown mating inhibition of the native female in her nocturnal habitat. This paper reviews results of those studies and discusses some pertinent field be• havior ot H. zea and H. virescens as related to their pheromones.

Entomologists of the USDA-Agricultural Research cm x 30 cm piece of wood with wooden bases Service became actively interested in pheromone about 7 cm high at each end. Virgin Heliothis research for insects of economic importance in the females were secured in a heads-up, all wings late 1950s. The senior author's continuing associa• behind-the-back position with the clothes pins. In a tion with Heliothis pheromone research began in similar position, unmated males were secured with the early summer of 1960. At that time, a memoran• a clothes pin held in the sex-attractant tester's dum of instruction from a USDA-ARS chemist out• hand. Males were held in close proximity to the lined procedures by which field entomologists were secured females. If they attempted to curl their to determine the existence of a pheromone for abdomens toward the females, the presence of a Lepidoptera. Several wooden clothes pins separ• sex attractant was confirmed. These tests were ated by about 5 cm were attached to a 0.5 cm x 0.5 conducted in open laboratory space at the conven• ience of the entomologist. With the current knowl• edge of the relationship between Heliothis behavior *U.S. Department of Agriculture, Agricultural Research Service. and pheromone interactions one is understandably respectively: Southern Grain Insects Research Laboratory, Tifton, amused at those initial efforts to document the Ga; Cotton Insects Research Laboratory, Brownsville, Tex; South• existence of a Heliothis sex attractant. ern Grain Insects Research Laboratory. Tifton, Ga; and Cotton Insects Laboratory, Phoenix, Ariz, USA. Since those early beginnings, many significant

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. 291 a d v a n c e s have b e e n m a d e . T h i s paper reviews (1974) a n d T u m l i n s o n et al. (1975) identified Z-11 - m o r e t h a n 20 years of Heliothis p h e r o m o n e H D A L a n d ( Z ) - 9 - t e t r a d e c e n a l ( Z - 9 - T D A L ) a s the r e s e a r c h a n d explores the potential novel uses for p h e r o m o n e of H. virescens. Heliothis pheromones. Finally, Klun et al. (1979,1980a, 1980b) reported that H. zea females produce (Z)-7-hexadecenal (Z-7-HDAL), Z-11-HDAL, and hexadecenal. In Pheromone Identification addition to those aldehydes, H. virescens w e r e found to produce Z-9-TDAL, tetradecenal, and (Z)- Gentr y et al. (1964) d o c u m e n t e d the p r e s e n c e of a 11-hexadecenol (Z-11-HDOL). The pheromone sex attractant in ether extracts of w h o l e virgin mixtures a n d approximate m e a n percent c o m p o s i - f e m a l e s a n d / o r h e x a n e extracts of t h e last t w o tion of each component for each species, as abdominal segments of Heliothis virescens (F.). reported by Klun et al. (1979) are s h o w n in T a b l e 1. Berger et al. (1965) could not obtain active extracts, but demonstrated that male Heliothis zea (Boddie) a n d H. virescens entered e x t r e m e sexual activity w h e n e x p o s e d to certain g a s e s e m e r g i n g from the detector outlet of a gas liquid chromato• Table 1. Components and approximate percentage g r a p h i c ( G L C ) apparatus. T h e identification of of each comprising H e l i o t h i s z a e a n d H. virescens these p h e r o m o n e s w a s d e l a y e d for several years pheromones. b e c a u s e t e c h n i q u e s h a d not bee n d e v e l o p e d for Mean percentage rearing Heliothis spp in n u m b e r s large e n o u g h to C o m p o n e n t H. zea H. virescens collect t h e quantities of p h e r o m o n e n e e d e d for

identification. The development of procedures for (Z (-Hexadecenal 9 2 . 4 8 1 . 4 mass rearing Heliothis w a s b e g u n in 1967; Burton Hexadecenal 4 . 4 9 . 5 (1969) a n d Raulston a n d Lingren (1969, 1972) (Z )-9-Hexadecenal 1.7 1 . 3 h a v e reported on systems devised to m a s s rear H. (Z )-7-Hexadecenal 1.1 1 . 0 zea a n d H. virescens, respectively. (Z )-9-Tetradecenal 2 . 0 Tetradecenal Several scientists researched the identification 1.6 3 . 2 of Heliothis p h e r o m o n e s a n d contributed to the (Z )-11-Hexadecen-1-ol literature on t h e subject in the 1970s. M c D o n o u g h S o u r c e : K l u n e t a l . ( 1 9 7 9 ) . et al. (1970) reported partial structures of two com• p o u n d s b e l i e v e d to be sex p h e r o m o n e s of H. zea. O n e w a s thought to be a m o n o - u n s a t u r a t e d 1 4 - C alcohol, while the other w a s characterized as a Sparks et al. (1979b, 1979c) thoroughly field- mono-unsaturated 14-C acetate, probably trans-7- tested these c h e m i c a l c o m p o n e n t s a n d c o n c l u d e d tetradecen-1-ol acetate. that the mixtues containing all c o m p o n e n t s in the Jacobson et al. (1972), in a news release in approximate ratios identified from female oviposi• Chemical Engineering News, s u g g e s t e d that the tor w a s h e s by Klun et al. (1979) w e r e the phero• sex p h e r o m o n e for H. zea was cis-9-tetradecen-1 - m o n e s for H. zea a n d H. virescens. T h e y ol f o r m a t e ( Z - 9 - T D F ) . In a 1973 paper presentation determined that 133.6 ug of the four-component session at the national meeting of the Entomologi• p h e r o m o n e evaporated from a cigarette filter over cal Society of America, Sparks' summarized o n e night's activity period w a s about 7 5 % as effec• results of cooperative research with Dr. A.A. Sekul2 tive as four virgin H. zea females in capacity to of the Southern Grain Insects Research Labora• attract and lure males into traps. They compared tory, in w h i c h they c o n c l u d e d that (Z)-11 - the seven-component mixture against Virelure h e x a d e c e n a l ( Z - 1 1 - H D A L ) w a s a m a j o r (16:1 ratios, Z-11-HDALZ-9-TDAL) and H. vires• component of the H. zea pheromone. Roelofs et al. cens virgin females in tests located in Tifton, Geor• gia; Brownsville, Texas; and Phoenix, Arizona. Data 1 A.N. Sparks, 1973, Summary of progress in H. zea pheromone a v e r a g e d a c r o s s locations a n d three designs of research at Southern Grain Insects Research Laboratory traps s h o w e d that 1 2 2 . 4 µ g Virelure w a s about 4 0 % (Unpublished data.) Paper No. 63, ESA Meeting, Dallas, Tex, USA. as effective in c a t c h of m a l e s as four virgin females, and 151.8µg of the seven-component mixture was 2Currently at USDA-ARS, Southern Regional Research Laboratory, 1 3 5 % as attractive as females u s e d as bait. New Orleans, LA.

2 9 2 Heliothis Pheromones for females used as bait in traps. Several groups of Monitoring researchers (Snow et al. 1972; Hendricks et al. 1973; Roach 1975) made the comparison of index• ing populations of Heliothis spp in light traps vs The economic importance of Heliothis spp to agro• virgin female traps. Typical results are shown (Figs. nomic crops necessitates a readily available sys• 1, 2) in data presented by Roach (1975). These tem for monitoring the seasonal populations of data reconfirm that H. virescens is not very respon• these species. Light traps were the primary method sive to light traps while H. zea responds well. Light- of monitoring adult Heliothis spp populations prior trap catches may index seasonal fluctuations of to the use of traps containing virgin females or populations of H. zea more accurately than virgin synthetic pheromone as baits to lure and trap female traps; however, for both species, the data males. Walden (1942) presented the first compre• indicate that virgin female traps are more sensitive hensive report on seasonal occurrence and abun• to low populations early in the season and decline dance of the corn earworm, based on light-trap in efficiency with high populations late in the collections. Newcomb (1967) and Beckham(1970) season. used light traps to index the populations of H. zea Is there a possibility of monitoring both Heliothis a n d H. virescens, and reported that a significantly spp simultaneously in pheromone traps? Haile et lower percentage of the H. virescens populations al. (1973) used virgin females of both species responded to black-light lamps in traps than did H. together as lures for electric grid traps. They zea. However, Agee (1972) reported that both spe• reported catch reductions of 24.2% for H. virescens cies had similar ranges of sensitivity to emitted UV and 77.5% for H. zea over catches made with light. single-species lures. However, Roach (1975) sug• Virgin females were used as bait in traps to index gested that chemically synthesized pheromones populations of H. zea on the Island of St. Croix, U.S. might be used in the same trap, since the antago• Virgin Islands (Snow et al. 1968). Hendricks et al. nism was apparently behavioral. Since the struc• (1972) showed the utility of H. virescens virgin tures of the pheromones for H. zea a n d H.

70 H. vir. light trap catch H. vir. pheromone catch 60

0 21 28 5 11 19 26 2 9 16 23 30 7 14 21 28 4 11 18 2 5 1 8 15 22 29 6 13 20 27 3 10 17 21 A p r i l May June J u l y A u g Sept O c t N o v 1 9 7 2

Figure 1. Seasonal H. virescens light- and pheromone-trap catches at Pee Dee, SC, USA (Source: Roach 1972.)

2 9 3 7 0 0

6 0 0 H. zea l i g h t trap catch H. zea pheromone catch 500

4 0 0

3 0 0

2 0 0

100

21 28 5 11 19 26 2 9 16 2 3 30 7 14 21 28 4 11 18 2 5 1 8 15 22 2 9 6 13 20 2 7 3 10 17 21 A p r i l M a y J u n e J u l y A u g Sept O c t N o v 1 9 7 2

Figure 2. Seasonal H. z e a light- and pheromone-trap catches at Pee Dee, SC, USA. (Source: Roach 1972.)

virescens have b e e n d e s c r i b e d (Klun et al. 1979a, evaluated. Three types of traps—pie-plate sticky 1 9 8 0 a , 1 9 8 0 b ) , no reports have b e e n published of trap ( S n o w a n d C o p e l a n d 1969), w i n d - v a n e (Raul• their use together as lures in a single trap. ston et al. 1980), and electrocutor grid (Hollings- A l t h o u g h n u m e r o u s researchers use phero- worth et al. 1 9 6 3 ) — w e r e tested in Georgia, a n d a m o n e traps to obtain information on Heliothis spp, fourth t y p e — b a f f l e d c o n e — w a s tested in Arizona the relationship of trap c a t c h a n d actual popula• (Hollingsworth et al. 1978). T h e grid trap was the tions has not been determined. However, methods most efficient in capturing H. zea m a l e s lured to h a v e b e e n d e v e l o p e d over the past few years to within 1 meter of the trap in Georgia. Disregarding study t h e nocturnal behavior of adult Heliothis spp stimuli used as bait, the pie-plate, wind-vane, and (Lingren et al. 1978, 1 9 8 2 a , 1982b) a n d to relate grid traps c a p t u r e d an a v e r a g e of 5.7%, 27.5%, a n d behavior of the s p e c i e s to p h e r o m o n e s a n d other 57.5%, respectively, of all H. zea males lured to factors. Responses of male H. zea spp to phero- within 1 m of those traps. In the Phoenix test, disre• m o n e traps have b e e n s h o w n to be influenced by garding baits, t h e baffled-cone trap c a p t u r e d about trap location, type of trap, time of night within the 1 0 % as m a n y m a l e s as did the w i n d - v a n e trap. activity period, a g e structure a n d mating status of Raulston et al. (1980) compared catches of H. the population, a n d w e a t h e r p a r a m e t e r s (Sparks et virescens m a l e s in modified w i n d - v a n e a n d c o n e al. 1979a, 1979b; Raulston et al. 1979). traps. T h e w i n d - v a n e with half the floor r e m o v e d was 4 2 % efficient, while the baffled c o n e c a p t u r e d 1 1 . 4 % of males responding. Naturally, stimuli used as bait in traps resulted in Heliothis Pheromones for significant differences in male catch. Virelure cap• Population Suppression tured about 4 0 % a s m a n y m a l e s a s did virgin females and the total-complement pheromone c a p t u r e d about 1 3 5 % as m a n y m a l e s as did virgin Population Suppression via Traps females (Sparks et al. 1979a). T h e s a m e data s h o w that males respond differently to pheromone- Sparks et al. (1979a, 1979b) field-tested the Helio• baited traps, d e p e n d i n g u p o n time within the nor• this pheromones identified by Klun et al. (1979). mal nocturnal activity period. For example, T h e effects of several factors on trap c a t c h w e r e Heliothis virescens males do not r e s p o n d to

2 9 4 p h e r o m o n e - b a i t e d traps prior to entering their nor• published results of a study in w h i c h field e m e r • mal searching-for-mates behavior pattern. Virgin gence, collection of single insects, collection of females and the seven-component pheromone mating pairs, and males caught in p h e r o m o n e traps c a p t u r e d males most efficiently during the early were observed and graphed (Fig. 3). Note that peak part of the sexual activity period; relative efficiency e m e r g e n c e a n d peak mating o c c u r r e d 8 to 9 days decreased with length of time after initiation of this prior to peak capture in p h e r o m o n e traps. sexual activity period. T h e grid trap is the most efficient in c a t c h of Heliothis spp males will readily respond to s y n • Heliothis males (about 60%) lured to within 1 m, but thesized pheromones, and cone, wind-vane, and impractical because of power supply demand. electrocutor-grid p h e r o m o n e traps are c a p a b l e of Thus, if a mass-trapping control program were capturing hundreds of male Heliothis spp per trap initiated, a trap (wind-vane or cone) less than 4 5 % per night. Our data s h o w they do so on o c c a s i o n in efficient would have to be used. Further, males late season, w h e n high populations are present respond to pheromone traps most actively approxi• (unpublished data). However, Raulston et al. (1979) mately 1 week after peak e m e r g e n c e a n d peak

Capture/trap (n:1158) 20 M a t i n g pairs (n:319) Virgin females (n:95)

8 13 18 2 3 28 2 7 12 17

J u l y A u g u s t

Figure 3. The Interrelationship of collections of Heliothis virescens virgin females, mating pairs, and males in virgin female traps during one generation in a cotton field. (Raulston et al. 1979).

2 9 5 m a t i n g ; therefore it is highly unlikely that a m a s s - Sekul et al. (1975) p l a c e d µg quantities of Z-11 - t r a p p i n g p r o g r a m w o u l d ever be s u c c e s s f u l in re• H D A L on cigarette filters near virgin f e m a l e s u s e d m o v i n g a high p e r c e n t a g e of Heliothis m a l e s f r o m a as bait in traps a n d f o u n d that as little as 50 ug of the population in time to prevent mating, oviposition, cis isomer inhibited male c a t c h m o r e t h a n 9 9 % . and larval infestations. The trans isomer at the same rate produces only Knipling a n d M c G u i r e (1966) m a d e theoretical 1 1 % inhibition. T h e s e authors s u g g e s t e d that this c a l c u l a t i o n s b a s e d o n trap competitiveness, m o th naturally occurring chemical, Z-11-HDAL, might emergence patterns, survival rates, and protandry be u s e d as a mating disruptant b e c a u s e of the a n d c a l c u l a t e d that an initial trap.female ratio of at behavioral effect on c o r n e a r w o r m males. least 5:1 w o u l d be n e e d e d to obtain 9 5 % s u p p r e s • G a s t o n et al. (1967) w e r e t h e first to obtain sion of m a t i n g. B a s e d on current k n o w l e d g e of experimental confirmation that the premating com• Heliothis behavior, inefficiency of currently munication between the sexes could be disrupted d e s i g n e d traps, a n d our inability to formulate t h e by p e r m e a t i n g the a t m o s p h e r e with an insect aldehyde-type pheromones for proper release over pheromone. Their demonstration was with Tricho- an e x t e n d e d period of time, the future for effectively plusia ni (Hubner) in 27 m2 plots in w h i c h a virgin- mass trapping Heliothis s p p d o e s not look f e m a l e trap w a s d e p l o y e d a m o n g 100 planchets promising. from w h i c h 17 mg (about 17 0 0 0 f e m a l e equival• ents) of synthetic pheromone per planchet were Population Suppression via Air e v a p o r a t e d . T h e criterion w a s reduction of male Permeation c a t c h in the virgin-female trap. Mitchell et al. ( 1 9 7 5 , 1 9 7 6 ) at the Insects Attrac- Beroza (1960) w a s the first to suggest permeating tants, Behavior, and Basic Biology Laboratory the a t m o s p h e r e of c r o p e n v i r o n m e n t s with sex reported highly succesful results in attempts to p h e r o m o n e s to disrupt mating, prevent r e p r o d u c • disrupt mating of H. zea a n d H. virescens with tion, a n d r e d u c e infestations of e c o n o m i c a l l y d a m • Z - 9 - T D F a n d Z-11 - H D A L . In o n e test, they p l a c e d a g i n g insect pests. Knipling (1979) r e v i e w e d the virgin f e m a l e s in traps in the middle of an 81 m2 plot, theory a n d m o d e l e d the potential use of the air- s u r r o u n d e d those traps with 16 polyethylene c a p s p e r m e a t i o n t e c h n i q u e as a m e t h o d of control. containing 25 mg of test c h e m i c a l releasing 3 0 0 Rothschild (1981) summarized the developments u g / m i n per cap, a n d m e a s u r e d disruption of p h e - and prospects for mating disruptions with Lepidop- romonal communication by reduction of male tera. His review noted 170 mating-disruption trials, c a t c h in virgin-female traps operated in the c h e c k of w h i c h 2 5 % w e r e classified as s u c c e s s f u l in vs the treated plots. decreasing crop infestations and 75% as explora• With these experimental procedures, disruption tory. In m o r e t h a n 4 0 % of t h e trials, reduction of for H. zea a n d H. virescens was m e a s u r e d a b o v e male c a t c h at p h e r o m o n e or virgin f e m a l e sites w a s 95% when Z-9-TDF was dispensed. In another test, the sole criterion for disruption. In about 5 0 % of similar t e c h n i q u e s w e r e e m p l o y e d , with the e x c e p • these trials, success was measured by responses tion that laboratory-reared females with clipped of males to tethered, c l i p p e d - w i n g or otherwise wings w e r e p l a c e d in the center of plots in c a g e s d e c o y e d f e m a l e s in forest insect trials, a n d about that permitted mating. In this test, H. zea mating 2 5 % in field a n d o r c h a r d insect trials. T h u s , in the was reduced 96.7% by Z-9-TDF and 85.5% by majority of c a s e s , the mating status a n d behavior of Z - 1 1 - H D A L , while H. virescens mating w a s native females were completely ignored, although reduced 81.2% by Z-9-TDF and 95.8% by Z-11 - these are the most important parameters for e v a • HDAL. luating the s u c c e s s of mating disruption with highly M c L a u g h l i n et al. (1981) reported results of H. mobile Lepidoptera. zea mating-disruption studies in Florida. They Knipling a n d M c G u i r e (1966) c o n s t r u c t e d s e v e n e v a p o r a t e d Z - 1 1 - H D A L , Z - 9 - H D A L , a n d Z - 7 - hypothetical models to demonstrate principles H D A L , individually a n d in c o m b i n a t i o n , to c o m p a r e involved in the use of living insects or extracts with Z - 9 - T D F as mating disruptants. R e d u c t i o n of containing insect pheromones to control low-level c a t c h of males in a trap baited with the four- populations. Several field trials involving Heliothis c o m p o n e n t H. zea p h e r o m o n e a n d located in the spp and their pheromones, components of their center of 1 0 0 - m to 3 0 0 - m plots w a s the criterion for pheromones, or pheromone mimics have been disruption. T h e y c o n c l u d e d Z-11 - H D A L w a s the c o n d u c t e d , a n d brief discussions of those follow. disruptant of c h o i c e .

2 9 6 Carpenter and Sparks (1982a) tested all compo• 100 nents individually and mixtures of the components DM of the H. zea pheromone in a wind tunnel to deter• CF mine which, if any, of the compounds served as a 7 5 close-range attractant. They suspected that one of the minor components, based on percent of total pheromone, might serve as a close-range attrac• 50 tant and could serve as a potent mating inhibitor. They found that Z-11 -HDAL was the most attrac• tive of all the components, but that male moths were able to discern "preferred" components 25 and/ or mixtures of components in the presence of other components and mixtures. These data sug• gest that suppression of H. zea mating by confusing males through air permeation with less than the 2 4 8 12 16 24 full-complement pheromone is not a viable Distance between stimuli (cm) possibility. Figure 4. Comparison of Heliothis zea male Beroza (1972) and Knipling (1976) agreed that moth response to a dead H.zea male moth (DM) the degree of inhibition of mating by disruption of pinned to a cigarette filter and a cigarette filter the pheromone communication system would be (CF) without a male moth, both of which were decreased if the target insect possessed supple• inoculated with 100 ug of H. z e a female sex mentary mate-detection mechanisms other than pheromone and placed in a fine across the air pheromone signals. Carpenter and Sparks (1982b) flow in a wind tunnel allowing the formation of studied the effects of vision on the mating behavior individual pheromone plumes. of the male corn earworm moth. All tests were conducted in a wind tunnel (0.91 x 0.91 x 2.5 m) mounted on wheels and stationed in a cotton field. Male moths were allowed a choice of mock female MF CF + 100 µg pheromone vs cigarette filler impregnated with 100 µg pheromone; dead H. zea male m o t h + 100 pheromone vs filter + pheromone; and mock female vs filter with pheromone. Male moths selected mock females and dead males pinned to 7 5 cigarette filters containing 100 µg pheromone over cigarette filters impregnated with 100 ug phero• mone when separation distances of up to 16 cm were involved (Fig. 4). The maximum distance at 50 Fig. 4 which male H. zea can orient visually was calculated to be 16 to 22 cm. When mock females (no pheromone) were compared with 100 ug 2 5 pheromone impregnated in a cigarette filter, males preferred the mock female at a separation distance of 4 cm and the filter-pheromone at separation distances of 8 to 12 cm (Fig. 5). Pheromone- 2 4 8 12 stimulated males flying upwind in a pheromone Distance between stimuli (cm) plume were observed leaving the plume to veer toward the mock female only to return to the phero• Figure 5. Comparison of Heliothis zea male mone plume when the two lures were separated by response to a cigarette filter (CF) inoculated 12 cm. These data show that H. zea m a l e s use with 100 µg of H. zea female sex pheromone and visual cues in their mate-searching behavior. a mock female moth (MF), both placed in a line Generally, the effect of mating disruptants is transverse to the air flow in a wind tunnel allow• conveniently measured by evaporating test chemi• ing the formation of individual pheromone cals into the air around a trap baited with synthetic plumes.

2 9 7 pheromone or virgin female, and comparing 20, and 40 pairs per cage were released. Phero• catches of males in treated vs control area. This mone rates of 3.7, 37, and 370 g/ha were technique overlooks the behavioral aspects, popu• dispensed on 100 cigarette filters per cage lation density, population movement, age of (3700/ha). Laboratory tests indicated that the esti• insects, mating status of insects, and the ability of mated quantity of pheromone evaporating after 7 feral females within the test area to secure a mate. hours w a s approximately 1 3 % . In the summer of 1979, A.N. Sparks and J.E. Mating data from tests run in early vs late season Carpenter (unpublished data) planted cotton in 9 x with no pheromone treatments showed highly sig• 30 x 4.1 m Saran® screen-covered cages. From nificant differences in percentage of the population the time the cotton began fruiting until early fall, a mating. Regardless of population released in the series of disruption studies was conducted. Helio- cage, early-season mating averaged approxi• this spp pheromone components were impreg- mately 70%, while late-season mating averaged nated individually and in mixtures in cigarette filters about 30%. The mating observed ranged from that were later stapled to cotton plant terminals. 32.5% to 35.0% to 15.0% for the 3.7, 37, and 370 Rates of pheromones applied were 186 mg, 18.6 g, g/ha treated plots, respectively, when 10 pairs and 186 g/ha. Laboratory-reared males and were released per cage (Table 2). When 40 pairs females were released at opposite ends of the per cage were released, mating ranged from 45.0 cage and observed for mating. Numbers of pairs to 52.5% to 29.4% for the 3.7, 37, and 370 g/ha released ranged from 50 to 100 per cage per test treatments, respectively. These data do show sig• night. Pheromone-impregnated filters were used nificant differences in percent mating observed at only on one test night. In these tests, mating was varying densities of insects subjected to this range never significantly inhibited, although the 186 g/ha of applied pheromone treatments. However, in no rate of the full-complement H. virescens p h e r o • case could successful inhibition of mating be mone delayed the onset of mating for approxi• claimed. Finally, in this series of tests, only five pairs 1 mately 1 to 1 /2 hr. per cage were released after application of 37 g/ha Beroza and Knipling (1972) postulated that the of full-complement H. zea pheromone or (Z)-11 - effectiveness of the air permeation technique hexadecenal. This late-season test showed wide would be influenced by population density. Criti• variation in mating, but indicated some possibility cism of the numbers of insects released encour• for reducing mating of extremely low populations of aged Carpenter et al. (1982) to repeat the H. zea with a high concentration of pheromones (37 experiment, using wider dosage ranges of phero• g / h a ) . mone and releasing fewer numbers of insects. Commercial efforts have been made to disrupt Without applying pheromone, they established no Heliothis spp mating. In late-season 1979, Lingren significant differences in mating of H. zea in three et al. (1982) observed and evaluated one such trial. cages (9 x 30 x 4.1 m) planted to cotton when 10, A large field of cotton (ca. 230 ha) had been treated

Table 2. Mean percentage of mating at three populatio n levels of Heliothis zea on cotton in field cagas containing pharomona Altar.a

Mean percent mating ( SE)b with pheromone level of

Population level 3 . 7 g / h a 3 7 g / h a 3 7 0 g / h a (pairs/cage) 30 June-3 July 23 June-26 June 7 July-10 July

1 0 3 2 . 5 1 2 . 6 b 3 5 . 0 1 9 . 2 b 1 5 . 0 1 0 . 0 a 2 0 5 8 . 8 1 4 . 4 a 5 2 . 5 1 2 . 6 a 2 7 . 5 1 5 . 6 a 4 0 4 5 . 0 2 0 . 7 a b 5 2 . 5 1 4 . 0 a 2 9 . 4 1 0 . 5 a

a. The 9 x 30 m screen field cages were planted with cotton and 100 cigarette filters contain• ing 3.7, 37, and 370 g/ha of pheromone were evenly s paced throughout the cages. b . Means followed by the same letter in each column ar e not significantly different at 5%

level, Duncan's multiple range test.

2 9 8 four or five times with 8.7 g / h a per application of population h a d b e e n annihilated by the insecticide the s e v e n - c o m p o n e n t H. virescens pheromone. treatment. No mating pairs w e r e f o u n d in either T h e cotton a p p e a r e d to have been fruiting well field, further supporting the conclusion that sexu• throughout t h e s e a s o n a n d s h o w e d very little d a m • ally mature insects had beeen killed by the insecti• age. A nearby 3 2 - h a field w a s used as a c h e c k . cide application. With these data in mind a n d On the night following the sixth application of considering the large quantitative differences p h e r o m o n e (Table 3), we evaluated c h e c k (C) a n d observed on this night, resulting in an adult c a p • treated (T) fields from 2 1 0 0 to 0 4 3 0 hr. We t u r e / m a n hour of 1.8 in the T a n d 15.2 in the C field, observed two completely different adult popula• it is clear the C field had received infestation pres• tions. T h e C field adult population c o n t a i n e d t w i c e sure the previous generation, while the T field h a d as many males as females with a virginity rate of not. 9 3 % . T h e T field had an equal male:female ratio Observations (2400-0430 hr) the fourth night fol• with a virginity rate of 13%. Most of the adults lowing p h e r o m o n e application bega n to indicate collected as singles in the C field were extremely " r e c o v e r y " of the population from the insecticide docile a n d easily collected. S u c h docile adults are application 72 hours previously and indicate a rela• normally freshly e m e r g e d a n d have not m a d e an tively homogeneous population in the T and C initial flight. The population observed and collected fields. Recalling that the " o l d " population observed in the T field w a s indicative of " o l d " population. T h e initially in the T field had been annihilated by the sex ratio was 1:1, a n d single collected females insecticide application, it now appears that young, a v e r a g e d 1.8 but ranged up to five previous mat- sexually mature adults h a d begun moving into the ings. In view of the lack of insect pressure in the field as indicated by the high percentage of female previous generation, these adults had probably virginity and the increase in mating. A similar pat• m o v e d into the field. This is a striking e x a m p l e of tern was observed in the C field, a n d the reduction the population differences that may be encoun• in virginity in this field in c o m p a r i s o n with the pre• tered even in adjacent fields. In programs dealing vious observation nights indicated that the pre• with mobile adult insects, s u c h e x a m p l e s d e m o n • p o n d e r a n c e of e m e r g e n c e had occurred, the strate the n e e d for a c o m p l e t e a n d t h o r o u g h adults were now dispersing, and the population a s s e s s m e n t of in-field wild populations in t e r m s of was beginning the " a g i n g " process. This c o n c l u • their sex ratio and age structure as a prerequisite to sion is further demonstrated by a return to a 1:1 sex program evaluation. ratio resulting from dispersal. Besides these qualitative differences in the age Observations on night 4 again indicated that the structure, the t w o populations also exhibited q u a n • p h e r o m o n e treatment had no effect on H. vires• titative differences. T h e larger population w a s cens mating in the field. In fact, considering differ• present in the C field, as indicated by the c a p t u r e / e n c e s in population density, as indicated by the m a n hour data presented in T a b l e 3. Only five a n d single insect c a p t u r e / m a n hour, more mating w a s three mating pairs were collected, respectively, in observed in the p h e r o m o n e field than in the c h e c k the C a n d T fields. Considering the quantitative field. This difference is probably not significant differences o b s e r v e d b e t w e e n the populations, no w h e n the population sources in the two fields are significant differences in mating c a n be a s s i g n e d considered. T h e population in the C field probably b e t w e e n T a n d C fields on night 0. During the had a residual emergence occurring; thus for a unit afternoon following t h e first night's observations, all of population there were m o r e sexually i m m a t u r e fields w e r e treated with a mixture of methyl para- adults in this field than in the T field, w h i c h c o n • thion, acephate, and chlordimeform insecticides. sisted almost totally of sexually mature insects that We o b s e r v e d f r o m 2 4 0 0 to 0 4 3 0 hr, about 24 hours m o v e d into the field. after the insecticide application, a n d the data rein• Observations reported here are not meant to be f o r c e d the population a s s e s s m e n t s w e had m a d e taken as an absolute evaluation of the program. t h e previous night. T h e " o l d " population in t h e T They simply address the inherent pitfalls of eva• field was effectively annihilated, and the few adults luating s u c h a program without intensive o b s e r v a • that w e r e o b s e r v e d were freshly e m e r g e d , as indi• tions on the adult population a n d the inferences c a t e d b y the 1 0 0 % female virginity. T h e e m e r g i n g that c a n b e d r a w n from s u c h observations. C o n • population in t h e C field h a d a male:female ratio of sider the use of infestation records. T h e d a t a c o l • 7.4:1, indicating that the population h a d p a s s e d the lected on night 0 indicated a heavily m a t e d emergence peak and that the previously emerged population in the T field. Considering t h e maturity

2 9 9 T a b l e 3 . Q u a n t i t a t i v e , o b s e r v e d , 0 - , 2 - , a n d 4 - d a y d i f f e r en c e s i n a f f e c t s o f 8 . 7 5 g / h a s e v e n - c o m p o n e n t H e l i o t h i s virescens pheromone formulatad in the C o n r e l f i b e r , a p p l i e d b y p l a n e t o a 2 3 0 - h a f i e l d o f c o t to n I n P h o e n i x , A r i z , U S A .

R a t i o o f single hourly capture:

T o t a l R a t i o V i r g i n A v e r a g e Capture/man t o t a l m a t i n g p a i r c a p t u r e male:female f e m a l e s spermatophore h o u r c o l l e c t i o n

(%)

N i g h t 0

T r e a t e d S i n g l e s 3 0 1:1 1 3 . 3 1 . 8 5 1 . 6 : 1 M a t i n g P a i r s 3 - 0 2 . 3 -

U n t r e a t e d S i n g l e s 4 1 1 . 9 : 1 9 2 . 9 0 . 1 8 . 2 1 . 6 : 1 M a t i n g P a i r s 5 - 2 0 1 . 8 -

N i g h t 2

T r e a t e d S i n g l e s 7 2 . 5 : 1 1 0 0 0 1 . 8 M a t i n g P a i r s 0 - - -- -

U n t r e a t e d S i n g l e s 7 6 7 . 4 : 1 1 0 0 0 1 5 . 2 M a t i n g P a i r s 0 - - - - -

N i g h t 4

T r e a t e d S i n g l e s 3 1 : 1 1 0 0 0 1 0 . 2 : 1 M a t i n g P a i r s 5 - 6 0 0 . 4 -

U n t r e a t e d S i n g l e s 1 0 1 : 1 6 0 0 . 4 3 . 3 0 . 4 : 1 - M a t i n g P a i r s 7 1 0 0 0 -

Source: Lingren et al. (1982), in part. a n d attractiveness of this cotton crop, had the male response to the s e v e n - c o m p o n e n t phero• heavily m a t e d population been of a d e q u a t e size, mone, a n d trap capture. T h e greatest effects w e r e tremendous infestation pressure would have been observed when either the full-complement phero• exerted on the T field, regardless of w h e r e the m o n e or Virelure was dispensed in the treated plot. mating h a d o c c u r r e d . Under these c i r u m s t a n c e s , A concentration of 372 m g / h a of these materials infestation records would yield little information reduced mating for the clipped-wing females by c o n c e r n i n g the effect of the treatment on the target about 9 0 % , and male response to the single p h e r o • behavior (mating) a n d c o u l d indeed result in c o n • m o n e source by 100%. In addition, the 372 m g / h a clusions diametrically opposed to the true situation. concentration of Virelure r e d u c e d trap capture Two other techniques used for pheromone dis• 100%; the trap response s h o w n for the s e v e n - ruption evaluation, a n d perhaps the least under• c o m p o n e n t p h e r o m o n e was obtained from a trap stood are traps a n d mating tables, or variations located 10 m d o w n w i n d of the treated plot, a n d this thereof. Certainly, assessment of Heliothis p o p • may have resulted in the increased capture noted ulations through trap-capture data is very poorly in this instance. understood b e c a u s e of the n u m b e r of variables Dispensing individual components of the that affect trap capture, including (1) trap effi• t o b a c c o b u d w o r m p h e r o m o n e h a d less effect; ciency, (2) weather, (3) age structure of the popula• none reduced mating of the clipped-wing females tion, a n d (4) attractant used to effect capture. All of by more than 55%. In most instances there w a s a these variables have a direct influence on our abil• greater reduction in male response to a single ity to decipher the m e a n i n g of trap capture as it p h e r o m o n e source than in clipped-wing female relates to p h e r o m o n e disruption. We c a n capture mating. This trend was also evident in the effect of males in traps with s e m i o c h e m i c a l s , but we do not the single c o m p o n e n t s on trap capture. Indeed, have the ability to relate c a t c h in a positive manner, 1240 m g / h a of Z - 9 - T D A L r e d u c e d trap capture either qualitatively or quantitatively, to mating of about 9 9 % , while almost half of the c l i p p e d - w i n g wild insects in a p h e r o m o n e - t r e a t e d area. Another females were able to obtain mates. T h e r e w a s no limitation of traps a n d mating tables in p h e r o m o n e reduction in wild female matings as indexed by the disruption assessment is their inability to sample number of pairs collected in the treated a n d the wild female population, the most important untreated plots. Clearly, there is no relationship aspect of the entire program! Further, in e s s e n c e b e t w e e n the clipped-wing female matings a n d trap e a c h trap a n d e a c h mating table emits o n e phero• captures. m o n e p l u m e a n d is of little more value t h a n a single Observations with night-vision goggles were sexually mature female as an evaluation tool, for if m a d e of males responding to the single s o u r c e of o n e male responds to a point s o u r c e of p h e r o m o n e s e v e n - c o m p o n e n t p h e r o m o n e located in the c e n • (female, trap, or table), mating at that particular site tre of the plot treated with t h e individual c o m p o • is indicated. nents. Males that r e s p o n d e d to the p h e r o m o n e The techniques and tools listed here should not s o u r c e were observed entering the p h e r o m o n e be e x c l u d e d from p h e r o m o n e evaluation, but c o n • plume, turning 90° upwind toward t h e source, clusions d r a w n from t h e m should be evaluated in a p p r o a c h i n g a n d in many instances m a k i n g c o n • the light of intensive nocturnal field observations. It tact with the source with claspers extended. T h e s e is very difficult to draw correct conclusions without behavioral responses were identical to the having data on actual field mating, a n d so far we responses observed to the p h e r o m o n e s o u r c e in have not d e v e l o p e d a d e q u a t e m e t h o d s to m a k e the untreated area. T h e only identifiable response this assessment beyond actual in-field nocturnal differences w e r e quantitative a n d not qualitative, observation. w h i c h woul d suggest that, at least in small plots In the s u m m e r of 1979, Raulston (published in s u c h as we w e r e working in (0.4 ha), sexually active part, in Lingren et al. 1982) d i s p e n s e d Virelure, the males may be repelled by the chemicals rather seven-component H. virescens p h e r o m o n e , a n d t h a n confused. Certainly this is a point that must be e a c h c o m p o n e n t individually, to determine the addressed, for it is imperative to know the kinds of effects of H. virescens mating behavior in 0.4-ha behavior affected by our so-called mating- field plots. He impregnated 1 2 4 0 cigarette filters disruption techniques. with 186 to 1240 mg of test material per hectare. T a b l e 5 s h o w s data collected on the wild popula• Table 4 shows the effects of dispensing phero• tion in the treated a n d untreated plots. T h e adult mone components on clipped-wing female mating, singles collections were m a d e b e t w e e n 2 1 0 0 a n d

301 Table 4. Effect of dispensing pheromone components in cotton on mating of clipped-wing females, male response to point source of pheromone, and trap capture of Heliothis virescens.

Percent reduction in CIipped-wing C o n e . / h a f e m a l e Response to Trap C o m p o n e n t (mg) m a t i n g p h e r o m o n e c a p t u r e

Seven-component pheromone 186 69 100 100a Seven-component pheromone 372 90 100 67.3a Seven-component pheromone 1240 100 100 1 0 0 V i r e l u r e 372 8 6 . 8 100 1 0 0 Hexadecenal + Tetradecenal 16:1 372 9.1 55 2 5 a (Z ) - 1 1 - H e x a d e c e n a l 186 4 9 . 1 7 6 . 6 89.1 a (Z ) - 1 1 - H e x a d e c e n a l 3 7 2 4 4 . 4 7 6 . 7 57.4 ( Z ) - 1 1 - H e x a d e c e n a l 1 2 4 0 2 8 . 6 7 1 . 4 8 6 . 0 (Z ) - 9 - T e t r a d e c e n a l 372 9.1 7 3 . 0 7 3 . 9 (Z )-9-Tetradecenal 1 2 4 0 5 3 . 7 7 7 . 4 9 8 . 6 (Z)-9-Hexadecenal 1240 1 9 . 6 6 4 . 5 3 2 . 9 (Z ) - 7 - H e x a d e c e n a l 186 1 0 . 3 5 8 . 8 4 6 . 2 (Z)-7-Hexadecenal 372 3 1 . 1 0 54.6 (Z )-11 -Hexadecen-l-ol 1240 5 2 . 6 2 9 . 3 5 9 . 4

Source: Lingren et al. (1982) in part.

a. Traps located 10m downwind of treated and untreated p l o t s . Table 5. Effect of dispensing pheromone components on mating of native Heliothis virescensns.

Singles Collection C o n e . / h a N o . Females/ ha N o . M a l e s / h a Mating pairs/ha C o m p o n e n t (mg) T r e a t e d U n t r e a t e d T r e a t e d U n t r e a t e d T r e a t e d U n t r e a t e d

Seven-component pheromone 186 17 2 2 9 17 0 7 . 5 Seven-component pheromone 3 7 2 8 22 8 37 0 7 . 5 Seven-component pheromone 1240 105 8 2 98 7 4 2 . 5 7 . 5 V i r e l u r e 3 7 2 6 0 8 2 119 82 1 0 . 0 0 •Hexadecenal + Tetradecenal 16 : 1 3 7 2 15 7 4 30 30 7 . 5 7 . 5 (Z)-11-Hexadecenal 186 120 96 8 3 6 8 16.9 7 . 5 (Z)-11 -Hexadecenal 3 7 2 179 128 114 8 2 5.0 3 0 . 0 (Z)-11-Hexadecenal 1 2 4 0 8 2 6 0 143 7 4 6 9 . 4 0 (Z )-9-Tetradecena I 372 53 6 0 15 98 7 . 5 2 . 5 (Z ) - 9 - T e t r a d e c e n a l 1240 113 37 6 0 37 1 0 . 0 0 (Z)-9-Hexadecenal 1240 22 30 0 11 0 0 (Z ) - 7 - H e x a d e c e n a l 186 128 68 150 6 8 2 4 . 8 7 . 5 (Z ) - 7 - H e x a d e c e n a l 3 7 2 120 7 4 150 115 3 0 . 0 1 5 . 2 (Z)-H-Hexadecen-l-ol 1240 113 143 53 8 3 1 2 . 4 7 . 5

Source: Lingren et al. (1982), in part. 2400 hr during the major feeding and ovipositing Heliothis Pheromones: periods and indicate no consistent quantitative dif• Potential for Novel Uses ferences between the treated and untreated areas. The quantitative differences in singles collections Pheromones for Heliothis spp have been identified noted between components are due to population and are highly attractive to males of the species. cycles during the test period. Further, none of the Their efficiency in trapping attracted males over an treatments consistently reduced mating of wild extended period of time remains a problem of adults in the treated area; in many instances, chemistry, engineering, and entomology. Entomol• greater numbers of mating pairs were collected in ogists must learn more about Heliothis adult the treated than in the untreated area. These data behavior and cooperate with engineers to develop were inconsistent with the trap captures, which more efficient traps and with chemists to formulate were invariably reduced by the single-component long-lasting, highly attractive lures. Entomologists treatments. Again, this indicates the weakness of must learn more about Heliothis behavior to equate using trap-capture reductions as an index to dis• actual catch with population densities, i.e., how trap ruption of precopulatory behavior. catch is affected by population density, age, mating We concluded that at the concentrations tested, status, trap design, host plants, lure, and weather none of the individual components of the multicom- parameters. Only when these problems have been ponent tobacco budworm pheromone resulted in researched thoroughly can we research the poten• the confusion of the wild male. tial of traps to suppress Heliothis populations. Henneberry et al. (1981) studied mating disrup• The literature reveals that in cases where chemi• tion of pink bollworm and tobacco budworm in Ariz• cals are reported to be highly effective Heliothis ona, using 16 treated cotton fields of 16 ha each mating inhibitors or pheromonal communication and one 4-ha field as a check. Materials tested disrupters, the criterion for disruption has been the against the budworm included 1 -tetradecenal for• reduction of male catch in traps baited with virgin mate (TF), (Z)-9-T-tetradecen-1 -of formate (Z-9- females or pheromones. The real evaluation criter• TDF) and Virelure (Z-11-HDAL + Z-9-TDAL). A ion should be the effect of the disruptant on the total of 13 applications was made in which 269.6, behavior of the adult Heliothis population in the 158.7, and 142.7 g/ha of TF, Virelure, and Z-9-TDF field, with particular emphasis on the number of were applied, respectively. The "inhibitors" were females copulating. formulated in polymeric plastic laminated flakes The largest known field application of phero• that released from 22 to 92% of the chemicals in 7 mone in which nocturnal observations of effects to 28 days. Rates of chemical per application in have been conducted involved about 230 ha. This g/ha ranged thus: TF (12.4-30.1), Virelure (7.4- size plot may be entirely too small for successful 14.8), and Z-9-TDF (8.7-19.8). application of the concept of "inhibiting mating of Virelure gave the best reduction of male capture Heliothis populations." Callahan et al. (1972) in traps (21 of 30 sample dates), while TF and trapped H. zea in 15 traps mounted on a TV tower Z-9-TDF significantly lowered male budworm moth from 7.7 to 322.2 m throughout the growing season. catches on only 10 of 30 sample dates. These The catch of mated females averaged 39.4%. findings in 16-ha plots differ grossly from the sma l l - Sparks et al. (1975) and Sparks (1979) showed that plot tests of Mitchell et al. (1975,1976) and Lingren numerous species of insects of economic impor• et al. (1982). tance move on southbound cool fronts up to 160+ Through September, egg counts, egg hatch, and km into the Gulf of Mexico. Forty-six percent of H. larval counts were not statistically different in zea females captured in light traps during this treated vs check fields. In October, on two sam• movement through the northern Gulf of Mexico pling dates, more eggs were found in control fields. were mated. French and Hurst (1969), Sparks Nocturnal observations of the adult populations (1972,1979), and Raulston (1979) have presented of Heliothis spp revealed about twice as many H. more evidence to show that H. zea, H. virescens, virescens as H. zea adults. Mating of both species a n d H. armigera migrate for extended distances. was reduced the night following an afternoon appli• However, Phillips (1979) believes that the bollworm cation, but the percentages of females mating the complex that produces serious problems on occa• night before and night after were not affected. sion in Arkansas is a local product of that state. Number of spermatophores/female in treated vs Based on the above information, it is apparent control fields was not affected. that if the technique of permeating the air with

3 0 4 pheromones is to successfully inhibit mating of GASTON, L.K., SHOREY, H.H., and SAARIO, C.A. Heliothis spp, huge areas of Heliothis hosts must 1967. Insect population control by the use of sex phero• be treated. Again, entomologists must learn more mones to inhibit orientation between the sexes. Natu r e about Heliothis spp movement and behavior to 213 (5081): 1155. cooperate with engineers to develop suitable deliv• GENTRY, C.R., LAWSON, F.R., and HOFFMAN, J.D. ery systems and chemists to develop longer last• 1964. A sex attractant in the tobacco budworm. Journal ing, highly effective chemicals. of Economic Entomology 57: 819.

HAILE, D.G., SNOW, J.W., and GOODENOUGH, J.L. References 1973. Reduced capture of tobacco budworm and corn earworm males in electric grid traps baited simultane• AGEE, H.R. 1972. Sensory response of the compound ously with virgin females of both species. Journal of E c o • eye of adult Heliothis zea a n d H. virescens to ultraviolet nomic Entomology 66: 739-740. stimuli. Annals of the Entomological Society of Ameri c a HARTSTACK, A.W., WITZ, J.A., and BUCK, D.R. 65: 701 -705. 1979. Moth traps for the tobacco budworm. Journal of BECKHAM, CM. 1970. Seasonal abundance of Helio• Economic Entomology 72: 519-522. this spp in the Georgia Piedmont. Journal of the Georgi a HENDRICKS, D.E., GRAHAM, H.M., GUERRA, R.J., Entomological Society 5: 138-142. and HARTSTACK, A.W., Jr. 1972. Catch of tobacco BERGER, R.S., McGOUGH, J.M., and MARTIN, D.F. budworm moth influenced by color of sex lure traps. 1965. S e x a t t r a c t a n t s of Heliothis zea a n d H. virescens. Environmental Entomology 1:48-51. Journal of Economic Entomology 58: 1023. HENDRICKS, D.E., GRAHAM, H.M., GUERRA, R.J., BEROZA, M. 1960. Insect attractants are taking hold. and PEREZ, C.T. 1973. C o m p a r i s o n s of n u m b e r s of Agricultural Chemistry 15: 37-40. tobacco budworms and bollworms caught in sex phero• mone traps vs blacklight traps in the Lower Rio Grande BEROZA, M. 1972. Insect sex attractant pheromones, a Valley, Texas. Journal of Economic Entomology 64: 361 - tool for reducing insect contamination in the envir o n m e n t . 3 6 4 . Toxicology and Environmental Chemical Review 1:109- HENNEBERRY, T.J., BARIOLA, L.A., FLINT, H.M., 134. LINGREN, P.D., GILLESPIE, J.M., and KYDONIEUS, BEROZA, M., and KNIPLING, E.F. 1972. G y p s y m o t h A . K . 1 9 8 1 . Pink bollworm and tobacco budworm mating control with sex attractant pheromone. Science 177:1 9 - disruption studies on cotton. Pages 267-283 in M a n a g e • 2 7 . ment of insect pests with semiochemicals: concepts an d practices, ed. E.R. Mitchell. New York, USA: Plenum BURTON, R.L. 1969. Mass rearing of the corn earworm Press. in the laboratory. U.S. Department of Agriculture, ARS 33-134, Washington, DC, USA. 8 pp. HOLLINGSWORTH, J.P., HARTSOCK, J.G., and STANLEY, J.M. 1963. Electric insect traps for survey CALLAHAN, P.S., SPARKS, A. N., SNOW, J.W., and purposes. U.S. Department of Agriculture, ARS 42-3-1 , COPELAND, W.W. 1972. Corn earworm moth: vertical Washington, DC, USA. 24 pp. distribution in nocturnal flight. Environmental Ent o m o l o g y 1 : 4 9 7 - 5 0 3 . HOLLINGSWORTH, J.P., HARTSTACK, A.W., BUCK, D.R., and HENDRICKS, D.E. 1978. Electric a n d CARPENTER, J.E., and SPARKS, A.N. 1982a. T h e non-electric moth traps baited with synthetic sex phero • specificity of Heliothis zea pheromone components in mone of the tobacco budworm. U.S. Department of Agr i • eliciting precopulatory responses from H. zea m a l e culture, ARS-5-173, Washington, DC, USA. moths. Journal of the Georgia Entomological Society (in JACOBSON, M., LANDIS, B.J., HENDRICKS, D.E., press). and PREISNER, E. 1972. Science concentrates. Chem• CARPENTER, J.E., and SPARKS, A.N. 1982b. Effects ical Engineering News. (Dec 4, 1972): 50. of vision on mating behavior of the male corn earwo r m KLUN, J.A., PLIMMER, J.R., BIERL-LEONHARDT, moth. Journal of Economic Entomology (in press). B.A., SPARKS, A.N., and CHAPMAN, O.L. CARPENTER, J.E., SPARKS, A.N., and GUELDNER, 1979. Trace chemicals: The essence of sexual com• R . C . 1982. Effects of moth population density and phero• munication systems in Heliothis species. Science 204: mone concentration on mating disruption of the com 1 3 2 8 - 1 3 3 0 . earworm in large screened cages. Journal of Economi c KLUN, J.A., PLIMMER, J.R., BIERL-LEONHARDT, Entomology (in press). B.A., SPARKS, A.N., PRIMIANI, M., CHAPMAN, O.L., FRENCH, R.A., and HURST, G.W. 1969. Moth immi• LEE, G.H., and LEPONE, G. 1980a. Sex p h e r o m o n e grations in the British Isles in July 1968. Entomologi s t ' s chemistry of female corn earworm moth, Heliothis zea. Gazette 20: 37-44. Journal of Chemical Ecology 6: 165-175.

3 0 5 KLUN, J.A., BIERL-LEONHARDT, B.A., PLIMMER, Heliothis zea (Boddie) and Heliothis virescens (F.) to light. J.R., SPARKS, A.N., PRIMIANI, M., CHAPMAN, O.L., M.S. thesis. Texas A&M University, College Station, T e x , LEPONE, G., and LEE, G.H. 1980b. S e x p h e r o m o n e USA. 59 pp. chemistry of the female tobacco budworm moth, Heliothis PHILLIPS, J.R. 1979. Migration of the bollworm Helio• virescens. J o u r n a l of C h e m i c a l E c o l o g y 6 : 1 7 7 - 1 8 3 . this zea (Boddie). Pages 419-441 in Movement of Highly KNIPLING, E.F. 1976. Role of pheromones and kairo- mobile insects: concepts and methodology in research, mones for insect suppression systems and their possib l e eds. R.L. Rabb and G.G. Kennedy. North Carolina Sta t e health and environmental impacts. Environmental Healt h University, Raleigh, NC, USA. Perspective 14:145-152. RAULSTON, J.R. 1979. Heliothis virescens migration. KNIPLING, E.F. 1979. The basic principles of insect P a g e s 4 1 2 - 4 1 9 in Movement of highly mobile insects: population suppression and management. Pages 421- concepts and methodology in research, eds. R.L. Rabb 4 8 8 in U.S. Department of Agriculture Agricultural Hand• and G.G. Kennedy. North Carolina State University, book 512, Washington, DC, USA. Raleigh, NC, USA.

KNIPLING, E.F., and McGUIRE, J.U., Jr. 1966. P o p u • RAULSTON, J.R., and LINGREN, P.D. 1969. A t e c h • lation models to test theoretical effects of sex attrac t a n t s nique for rearing larvae of the bollworm and tobacco used for insect control. U.S. Department of Agricul t u r e budworm in large numbers. Journal of Economic Ento• Agricultural Information Bulletin 308, Washington DC , m o l o g y 6 2 : 9 5 9 - 9 6 1 . USA. RAULSTON, J.R., and LINGREN, P.D. 1972. M e t h o d s LINGREN, P.D., SPARKS, A.N., RAULSTON, JR., of large-scale rearing of the tobacco budworm. U.S. and W O L F , W . W . 1 9 7 8 . Applications for nocturnal stu• Department of Agriculture Production Research Report dies of insects. Bulletin of the Entomological Societ y of 145, Washington DC, USA.10 pp. America 24: 206-212. RAULSTON, J.R., LINGREN, P.D., SPARKS, A.N., LINGREN, P.D., RAULSTON, JR., SPARKS, A.N., and MARTIN, D.F. 1979. Mating interaction between and WOLF, W.W. 1982a. Insect monitoring technology native tobacco budworms and released backcross for evaluation of suppression via pheromone systems . In adults. Environmental Entomology 8: 349-353. Insect suppression with controlled release pheromon e RAULSTON, JR., SPARKS, A.N., and LINGREN, P.D. systems, eds. G. Zewig, A.L. Kydonieus, and M. Bero z a , 1980. Design and cooperative capture of a wind-oriented Boca Raton, Florida, USA: CRC Press. (In press.) trap for capturing live Heliothis spp. Journal of Economic LINGREN, P.D., and WOLF, W.W. 1982b. N o c t u r n a l Entomology 73: 586-589. activity of tobacco budworm and other insects. In The role ROACH, S.H. 1975. Heliothiszea a n d H. virescens m o t h of biometeorology in integrated pest management, eds . activity as measured by blacklight and pheromone traps. J.C. Hatfield and IS. Thomason. New York, USA: Aca• Journal of Economic Entomology 68: 17-21. demic Press. (In press.) ROTHSCHILD, G.H.L. 1981. Current status and pros• MCDOUNOUGH, L.M., GEORGE, D.A., and LANDIS, pects for mating disruption of lepidopterous pests. P a g e s B.J. 1970. Partial structure of two sex pheromones of the 2 0 7 - 2 2 8 in Management of insect pests with semiochem• corn earworm, Heliothis zea J o u r n a l of E c o n o m i c E n t o • icals: concepts and practices, ed. E.R. Mitchell, Ne w Y o r k , m o l o g y 6 3 : 4 0 8 - 4 1 2 . U S A : P l e n u m Press.

MCLAUGHIN, JOHN R., MITCHEL, E.R., and ROELOFS, W.L., HILL, A.S., CARDE, R.T., and CROSS, J.H. 1981. Field and laboratory evaluation of BAKER, T.C. 1974. Two sex pheromone components of mating disruptants of Heliothis zea a n d Spodoptera trugi- the tobacco budworm moth Heliothis virescens. Life perda in Florida. Pages 243-251 in Management of insect Science 14: 1555-1562. pests with semiochemicals: concepts and practices. Ne w York, USA: Plenum Press. SEKUL, A.A., SPARKS, A.N., BEROZA, M., and MITCHELL, E.R., BAUMHOVER, A.H., and JACOB- BIERL, B.A. 1975. A natural inhibitor of the corn ear- SON, M. 1976. Reduction of mating potential of male worm moth sex attractant. Journal of Economic Entomol• Heliothis s p p . a n d Spodoptera trugiperda in field plots o g y 6 8 : 6 0 3 - 6 0 4 . treated with disruptants. Environmental Entomology 5: SNOW, J.W., and COPELAND, W.W. 1969. Fall a r m y - 4 8 4 - 4 8 6 . worm: use of virgin female traps to detect males and t o MITCHELL, E.R., JACOBSON, M., and BAUM• determine seasonal distribution. U.S. Department of A g r i • HOVER, A.H. 1975. Heliothis spp.: Disruption of phe- culture product research report 110, Washington DC, romonal communication with (Z)-9-tetradecen-1 -of U S A . 9 p p . formate. Environmental Entomology 4: 577-599. SNOW, J.W., CANTELO, W.W., BURTON, R.L., and NEWCOMB, D.D. 1967. Comparative behavior of adult HENSLEY, S.D. 1968. Population of fall armyworm, corn

3 0 6 earworm, and sugarcane borer on St. Croix, U.S. Virgin Islands. Journal of Economic Entomology 61:1757-1760.

SNOW, J.W., SPARKS, A.N., and LEWIS, W.J. 1 9 7 2 . Seasonal capture of corn earworm adults in light traps near Tifton, Georgia, compared with captures in traps baited with virgin females. Journal of the Geor g i a Entomological Society 7: 85-89.

SPARKS, A.N. 1972. Heliothis migration. In Distribution, abundance, and control of Heliothis species in cotton and other host plants. Southern Cooperative Series Bulletin 169, Oklahoma Agricultural Experiment Station, Okla• homa State University. Stillwater, Okla, USA. 92 pp.

SPARKS, A.N. 1979. An introduction to the status, cur• rent knowledge, and research on movement of selecte d Lepidoptera in Southeastern United States. Pages 382 - 3 8 5 in Movement of highly mobile insects: concepts and methodology in research, eds. R.L. Rabb and G.G. Kennedy. North Carolina State University, Raleigh, NC, USA.

SPARKS, A.N., JACKSON, R.D., and ALLEN, C.L. 1 9 7 5 . Corn earworms: Capture of adults in light traps on unmanned oil platforms in the Gulf of Mexico. Journal of Economic Entomology 68: 431 -432.

SPARKS, A.N., CARPENTER, J.E., and MULLINIX, B.G. 1979a. Field responses of male Heliothis zea ( B o d - die) to pheromonal stimuli and trap design. Journal of the Georgia Entomological Society 14: 318-325.

SPARKS, A.N., RAULSTON, J.R., LINGREN, P.D., CARPENTER, J.E., KLUN, J.A. and MULLINIX, B.G. 1979b. Field response of male Heliothis virescens (F.) to pheromone stimuli and traps Bulletin of the Entomolog i • cal Society of America 25: 268-274.

TUMLINSON, J.H., HENDRICKS, D.E., MITCHELL, E.R., and BRENNAN, M.M. 1975. Isolation, identifica• tion, and synthesis of the sex pheromone of the tobac c o budworm. Journal of Chemical Ecology 1:203-214.

WALDEN, H.H. 1942. Owlet moths (Phalaenidae) taken at light traps in Kansas and Nebraska. U.S. Departmen t of Agriculture, Circular 643, Washington DC, USA. 25 pp.

3 0 7

Practical Development of Pheromones in Heliothis Management

John R. McLaughlin and Everett R. Mitchell*

Abstract

The sex pheromones of Heliothis armigera, H. subflexa, H. virescens, and H. zea have been identified, and field-active synthetic pheromonal blends have been reported tor these species and tor H. punctigera. The greatest potential use tor these male attractants is in biomonitor• ing. Commercial formulations tor baiting traps are available, and reasonably efficient traps have been developed. At present, traps are used chiefly to detect males and monitor very gross changes in populations of adults. Further research is needed to utilize trap captures as a predictive tool to aid in pest-management decisions. Mass annihilation of males with traps is not considered a promising approach; however, the ability of sex pheromones to aggregate males may eventually prove useful. The air-permeation technique can be used to prevent mating of Heliothis, and can be integrated with all other control methods discussed at this workshop. The major obstacle to effective use of H e l i o t h i s pheromones in this manner is lack of a formulation that adequately protects and releases the aldehyde pheromonal components. Even it technological problems are solved, it is not clear that this method of control is economically feasible.

The sex pheromones of moths are such an impor• reviewed in recent works (Silverstein 1981, and tant element in reproduction that researchers have reviews cited therein). They tall into three broad long felt that they could be exploited as pest- categories of biomonitoring, mass annihilation of management tools. The potential uses of lepidop- attracted males, and disruption of mating commun• teran pheromones have been exhaustively ication via permeation of the air with pheromones or pheromone-like chemicals. The pheromonal *U.S. Department of Agriculture, Agricultural Research Service, mating communication system is also an important Insect Attractants, Behavior, and Basic Biology Research Labora• tory, Gainesville, Fla, USA. element in programs that rely upon the attraction

approach Potential Uses of Lepidopteran

Pheromones under wing

Biomonitoring

Meaningful biomonitoring requires an understand• hair pencil ing of the behavior of the insect and the chemicals utilized in pheromonal communication. Progress with Heliothis species has been slow, but in recent years the chemical messages of H. zea (Boddie), male H. virescens (F.), H. armigera ( H b n ) , H. subflexa fans female fans (Gn.), a n d H. punctigera (Wallgn.) have been worked out to the extent that field monitoring with synthetic chemical blends is possible (Table 1). moves At present, our knowledge of heliothid phero- parallel mones comes primarily from analyses of com• pounds extracted with organic solvents from the suspected pheromone glands. Elucidation of the

exact pheromone systems will occur by analysis of male female turns the compounds and ratios of compounds actually turns released into the air. Such research is difficult, but indications with U.S. species are that advances in our ability to attract or trap males can be expecte d (Teal, personal communication). clasp Efforts are under way to expand our understand• hoirpencil ing of the detailed chemical ecology of H. vires• cens, H. zea, and H. subflexa in the USA (Primiani 1979, Teal et al. 1981 a, Fig. 1), and it is hoped these Figure 1. Comprehensive ethogram of H. revelations will increase our ability to trap those virescens courtship behavior. (Source: Teal et species or interdict reproduction. al. 1981a.)

Table 1. Field-active sex pheromone components of H e l i o t h i s species..

Heliothis Chemical (Ratio) s p e c i e s Z11:16A1 Z9:16A1 Z 7:16A1 16A1 Z11:16Ac 9:16Ac Z 7: 16Ac Z 9:14A1

H. armigera ( 9 7 ) ( 3 ) ------H. punctigera ( 5 0 ) - ( 5 0 ) ( 1 ) - - H. subflexa ( 4 0 ) ( 3 0 ) - - (12) (6) (2) - H. virescens ( 1 6 ) - - - - (1) - H. zea (116) (5) (3) (11) - -

S o u r c e s : H e l i o t h i s armigera: Kehat et al. (1980); punctigera: Rothschild (1978) (not identified from female); subflexa: Teal et al. (1981b); virescens: Tumlinson et al. (1975)'; zea: Klun et al. (1979, 1980).

3 1 0 The major problem in biomonitoring, however, is was expanded (Shorey et al. 1976; Shorey 1977) to not in our ability to trap these insects, but in our include both misdirection and sensory fatigue inability to utilize the information obtained. There when a material that attracts males is used as the are as yet no reports in the literature of strong disruptant. These authors emphasized that dis• correlations of population relationships with trap orientation effects are not crucial, because many data, although Tingle and Mitchell (1981) have nonattractive chemicals are effective disruptants. reported some predictive data with pheromone Shorey and colleagues worked with what was traps for H. virescens in tobacco. believed at that time to be a monochemical pheromone system. Most lepidopteran sex pheromones Mass Annihilation are now known to be multichemical blends. Klun et al. (1973, 1975), while studying the multicompo- This approach has not been extensively nent pheromone systems of the European corn researched, probably because highly effective borer, Ostrinia nubilalis (Hiibner) and the red- attractants and efficient traps have not been deve• banded leafroller, Argyrotaenia velutinana loped. The logistical requirements for mass annihi• (Walker), proposed that the best strategy to lation projects are numerous, and this approach to achieve mating control might involve either the control of widespread field-crop pests has not been alteration of the chemical blend received by the appealing. Future development of highly virulent male or sensory fatigue causing loss of response to pathogens or other agents that might be spread by a pheromonal chemical responsible for very short- males or used to kill aggregated males may open range phases of mating communication. For exam• new possibilities for pheromonal manipulation. ple, with insects that depend upon specific ratios of geometric isomers for aggregation and mating, the Mating Disruption via Air Permeation most efficient approach might be to utilize the iso• mer present in the least amount in the pheromonal The most researched and most controversial use blend. of Heliothis sex pheromones has been their direct Roelofs (1978) hypothesized that the best dis• application as mating disruptants. Several hypo• ruptant should be that blend of chemicals most theses have been advanced as to how mating can closely tuned to the receptor system. Thus, the be eliminated by overloading the environment with degree of mating disruption achieved with a given an insect's sex pheromone. A male-confusion concentration (release rate) of a disruptant blend technique was proposed by Beroza in 1960 (Ber- should be in proportion to the degree to which the oza 1976), prior to the identification of any insect blend approximates the natural pheromone. sex pheromone. His hypothesis was that if a syn• Carde (1981) has proposed that pheromone thetic sex pheromone were emitted from many communication may be camouflaged by raising the dispersed particles, the males responding to the concentration of synthetic pheromone sufficiently pheromone would be unable to distinguish above that of the density emanating from the between the synthetic odor and that of the relatively female that the boundaries of the natural plumes few females present in the same area; thus no become indiscernible. Thus, one is not dealing with mating would occur. T h e m e c h a n i s m of effect is sensory fatigue or misdirection or competition, but that of misdirection of males in the presence of a with a system in which the message is so omni• large number of competing pseudofemales (Ber• present that a male cannot negotiate a typical zig- oza 1976). zag upwind course to a female. Research with the pheromone of the cabbage These are all appealing explanations for the phe- looper, Trichoplusia ni (H'ubner), established the nomenon of mating disruption. Since none of them feasibility of disrupting sex pheromone communi• appears to be universally true, research into the cation by distributing evaporators of the synthetic selection and application of mating disruptants in pheromone throughout cabbage fields (Gaston et field situations has been largely empirical. In the al. 1967; Shorey et al. 1967). G a s t o n a n d Shorey c a s e of Heliothis spp, research has been more realized that sensory thresholds must be affected confusing because the applied work was begun in the presence of physiologically large amounts of before the sex pheromones were reasonably well omnipresent pheromone, and hypothesized that defined by the chemists. An illustration of our pro• sensory adaptation and/or habituation would be gress (or lack of it, depending upon the critic) can the primary mechanism of effect. This hypothesis be made with the corn earworm, H. zea.

311 T h e feasibility of using t h e air-permeatio n t e c h • 1) pheromone-baited traps. The results with both nique for mating disruption of H. zea was demon• types of trap w e r e statistically equivalent a n d are strated by Mitchell et al. (1975,1976) using either pooled in T a b l e 3. T h e s e results w e r e possibly the pheromonal component, (Z)-11 -hexadecenal c o m p r o m i s e d to s o m e extent b e c a u s e the e x p e r i • (Z11:16A1), or a parapheromone, (Z)-9- mental spray equipment was not precise and there tetradecen-1 -ol formate (Z9:14F), dispensed from was undoubtedly some overspray that may have closed polyethylene vials. These materials were c o n t a m i n a t e d adjacent plots. T h e results indicated also effective against H. virescens. T h e c h e m i c a l s that the Z11:16A1 a n d Z9:14F w e r e equally effec• were tested concurrently for their effect on the tive as disruptants and as good as or better than the m a t i n g of c l i p p e d - w i n g virgin females in the field Z11:16A1 -Z9:16A1 mixture. Also, Virelure, the 16:1 a n d o n male c a p t u r e s i n f e m a l e - b a i t e d traps. T h e aldehyde mixture that is an effective trap bait for H. reductions in mating a n d in trap captures w e r e in virescens a p p e a r e d to be a g o o d disruptant for H. c l o s e a g r e e m e n t . zea. A microencapsulated formulation of Z9:14F also Testing to this point w a s intended to d e v e l o p a reduced mating in small test plots (Mitchell et al. disruptant a n d formulation that c o u l d be used in a 1976). However, a series of subsequent tests of larger scale experiment to control H. zea. T h e r e • mating disruptants formulated in various microcap• fore, in 1979, we also tested aerial application sys• sules, primarily in s o y b e a n s against the s o y b e a n t e m s for the plastic laminate flake a n d for hollow looper, Pseudoplusia includens Walker, and T. ni, fiber dispensers in 5.5-ha plots. T h e H. zea disrup• gave highly variable results, depending upon tant tested was Z9.14F, because the hollow fiber weather conditions (McLaughlin, unpublished system then in use was incompatible with Heliothis data). T h u s , this type of formulation w a s not c o n s i • aldehydes. This test ( M c L a u g h l i n et al. 1981) d e r e d reliable for large-scale field tests. established the hollow fiber s y s t e m as m o r e relia• In 1979, M c L a u g h l i n et al. (1981) c o n d u c t e d a ble a n d efficacious a n d thus the hollow fiber- series of experiments to identify the disruptant of Z9:14F formulation was chosen for a large-scale c h o i c e for H. zea. This r e s e a r c h w a s p r o m p t e d by test in 1980, e v e n t h o u g h the disruptant of c h o i c e developments in formulations for sex pheromones a p p e a r e d to be Z 1 1 : 1 6 A 1 . by the Albany International Company (hollow fiber During the s u m m e r of 1980 (Mitchell a n d dispensers) a n d the H e r c o n Division of Health- M c L a u g h l i n 1982), a 1 2 - h a field of c o r n w a s treated Chem Corporation (laminated plastic dispensers) with Z9:14F and a nearly identical 12-ha field less a n d by the breakthrough definition of the H. zea than 1 km away was treated with (Z)-9-tetradecen- p h e r o m o n e g l a n d contents by Klun et al. (1979, 1 -ol a c e t a t e (Z9:14Ac), a disruptant of fall a r m y - 1980, T a b l e 1). w o r m , Spodoptera frugiperda (J.E. Smith), sex The initial small-plot tests (100 m2 to 3 0 0 m2) in p h e r o m o n e c o m m u n i c a t i o n . T h e H. zea disruptant peanut fields using plastic laminate dispensers at• does not affect S. frugiperda a n d vice versa. T h e t a c h e d to stakes established that the major ovipos• Albany International system for aerially dispersing itor c o m p o n e n t , Z 1 1 : 1 6 A 1 , w a s a m o r e effective hollow fibers in a polybutene sticker w a s used to disruptant of mating c o m m u n i c a t i o n , m e a s u r e d via treat e a c h field at 7- to 9-day intervals. T h e H. zea reductions in t h e c a p t u r e of m a l e s in synthetic field received a total of 217.3 g of Z9:14F in six p h e r o m o n e - b a i t e d traps, t h a n the c o m p o n e n t s applications from 2 June to 9 July. This was 1975.3 Z9:16A1 or Z7:16A1 (Table 2). T h e activity of g of f o r m u l a t e d fiber ( 1 1 % Z9:14F). T h e S. frugi- Z11:16A1 was not significantly increased with the perda field received 183.7 g of Z 9 : 1 4 A c in a similar use of t h e p h e r o m o n a l mixture reported by Klun et formulation. al. ( 1 9 7 9 , 1 9 8 0 ) ; however, the blends of p h e r o m o • Data on mating w e r e collected on eight nights nal components were significantly more effective b e t w e e n 19 J u n e a n d 14 July. Using h e a d l a m p s , t h a n Z9:14F at the w i d e evaporator s p a c i n g (Table observers (two/field) walked through each field 2). a n d collected mating pairs of feral H. zea a n d S. A n additional test w a s c o n d u c t e d t o evaluate t h e frugiperda. B e c a u s e of the oviposition habits of S. potential of plastic laminate flake formulations of frugiperda, the observers w e r e also able to collect Heliothis aldehydes as H. zea disruptants. T h e s e S. frugiperda egg m a s s e s from the c o r n plants. materials were applied by air using a latex-based T h e s e examinations w e r e started at 2 4 0 0 hr a n d sticker ( M c L a u g h l i n et al. 1981). T h e tests w e r e c o n t i n u e d until 0 3 0 0 hr. T h e number of e g g m a s s e s e v a l u a t e d with f e m a l e - b a i t e d a n d synthetic (Table a n d mating pairs of the t w o species w e r e r e c o r d e d

3 1 2 Table 2. Mean (± 8E) captures of male H. zea In traps baited with synthetic pheromone (Table 1) and pl a c e d i n plots permeated with sex pheromone components evapo rated from 3.2 cm2 plastic laminates (16 evaporators/plot).

P e r m e a t i n g Plot size (m2 ) c h e m i c a l 1 0 0 3 0 0

Test 1 (16-20 July)

C o n t r o l 6 . 4 ± 3 . 0 Z 1 1 : 1 6 A 1 0 . 3 ± 0 . 1 Z 9 : 1 6 A 1 3 . 7 ± 0 . 9 Z 7 : 1 6 A 1 4 . 5 ± 4 . 8 1 6 A 1 1 5 . 7 ± 4 . 8

Test 2 (1-6 Aug)

C o n t r o l 43.8 ± 15.6 Z 1 1 : 1 6 A 1 6 . 6 ± 3 . 5 Z11:16A1 and Z9:16A1 (1:1) 9 . 0 ± 5 . 4 Z11:16A1 and Z7:16A1 (1:1) 9 . 6 ± 5 . 8

T e s t 3 (27-31 July) ( 9 - 1 3 A u g )

C o n t r o l 1 3 . 3 ± 2 . 5 3 7 . 5 ± 8 . 5 Z 1 1 : 1 6 A 1 1 . 2 ± 0 . 3 5 . 4 ± 1.8 Z11:16A1 and Z9:16A1 (1:1) 0 . 8 ± 0 . 3 2 . 7 ± 1 . 5 Z 9 : 1 4 F 2 . 1 ± 2 . 5 1 2 . 7 ± 3 . 5 CEW 4-component (trapping ratio) 2 . 1 ± 2 . 5 1 2 . 7 ± 3 . 5

Table 3. Captures of male H. zea In female-balted compared with mating in the field treated with traps placed In 0.81-ha plots of sweet corn treated b y Z9:14Ac is shown in Figure 2. Mating by S. frugi- air with mating disruptants (10 g al/plot). perda is shown in Figure 3. The average reduction in H. zea mating was 5 0 % ; that is S.frugiperda, 8 6 % .

M e a n / t r a p / Moreover, oviposition by S. frugiperda was r e d u c e d D a y s t o n i g h t 8 4 % . f i r s t m o t h (4 plots-14 Because these fields were surrounded by corn- C h e m i c a l c a p t u r e n i g h t s ) fields and other alternative hosts, these tests dem• onstrated that mating in both species could be influenced even in relatively small fields. Damage Z11:16A1 and by H. zea, however, was substantial, a n d m u c h of Z9.16A1 (1:1) 3 2 . 8 Z11:16A1 and that damage was probably due to larvae originating Z9:14A1 (16:1) 2 0 . 8 from females that mated within the test field. Z 9 : 1 4 F 1 4 0 . 4 The poor level of mating control achieved with H. Z 1 1 : 1 6 A 1 1 1 1.1 zea was possibly due to inefficient delivery of the C o n t r o l 1 4 . 7 material by the application system. Observations indicated that most of the fibers aerially applied to corn 15 to 24 cm high fall to the ground, and even in at 15-minute intervals (=1 replicate) throughout th e larger corn many fibers did not adhere to the plants. examination period. The equipment was calibrated to deliver at its maxi• M a t i n g b y H . zea in the field treated with Z9:14F m u m rate, and the treatment level w a s attained by

3 1 3 35

Control

30 TDF

2 5

0 6 7 59 46 ( + 4 3 ) 6 3 3 5 4 2 44

% Mating reduction (or increase) vs control

t t t t

16 19 2 3 26 30 3 7 10 14 J u n e J u l y Figure 2. Effects of Z9:14F (TDF) treatments on mating by corn earworm (H. zea) in a 12-ha field of corn. Dates of application indicated by "t."

20 C o n t r o l TDA

6 9 100 8 2 100 100 6 1 7 5 100

% Mating reduction vs. control

t t t t

16 19 2 3 26 30 3 7 10 14 J u n e J u l y

Figure 3. Effects of Z9:14Ac (TDA) on mating by fall armyworm (S. frugiperda) in a 12-ha field of corn. Dates of application indicated by "t."

3 1 4 flying each swath twice. Thus, higher rates with the the plants with light cotton thread glued to the same formulation were not investigated, even thorax. Impact was assessed by the reduction in though subsequent small-plot tests with Z9:14F trap capture or number of females that were mated dispensed from polyethylene vials attached to the relative to these parameters in the untreated con• corn plants reaffirmed that higher levels of com• trol plots (Table 4). The primary H. zea aldehyde, munication disruption than those obtained in the Z11:16A1 was about six times more effective in 12-ha field were possible using Z9:14F (Mitchell, reducing trap captures than was Z9:14F through• unpublished data). out the test and was at least three times as effective In the fall of 1980, the Albany International Com• in reducing mating by the fourth day of the test. pany brought a new black hollow fiber formulation The poor performance of the 16:1, Z11:16A1- to our laboratory for testing. A small-plot test indi• Z9:14A1, mixture was a disappointment. This cated, for the first time, a very marked difference would probably be the disruptant of choice for H. between the disruptive effects of Z11:16A1 (more virescens, and often one would wish to affect these effective) and Z9:14F. This was further investigated species simultaneously in the same crop. The in a set of small-plot tests conducted in soybean Z9:14A1 is not a disruptant of H. zea a n d may have fields in late summer of 1981. The method was acted as a diluent to reduce the evaporation of the similar to that employed in the 1979 screening active component, Z11:16A1, below the point tests. The test materials, in 25-fiber packets, were where it would be effective. A subsequent small- attached to wooden stakes set in a 6 x 6 grid (36 plot test with double the above rate of the H. vires• point sources/plot) with 3 m between stakes (plots cens 16:1 mixture and Z11:16A1 alone appeared to 15 m x 15 m). The estimated release rate of substantiate this (Table 5). Unfortunately, the Z11:16A1 from a hollow fiber is about 3.0 ng/min number of matings in the controls was small, and (Teal, personal communication), and this system thus further tests are needed. evaporated approximately 2700 ng of test material The results of past experiments (McLaughlin per minute per plot (7.1 mg/ha/hr). 1981) and the more recent tests presented here Each treatment was monitored using female- demonstrate that, excluding economic factors, the baited traps and virgin female moths tethered onto major obstacle to direct mating control of H. zea

Table 4. Percent of 10 tethered virgin female H. zeea that mated In a 225 m2 plot treated with pheromonal components evaporated from 36 stations In a 6 x 6 g rid (25 hollow fibers/station).

T r e a t m e n t Day ( R a t i o ) 2 3 4 5 8 9 1 0 1 1

C o n t r o l 1 0 0 1 0 0 8 6 8 6 7 0 7 5 7 8 7 5 Z 1 1 : 1 6 A 1 0 1 4 2 2 2 9 1 0 11 1 1 1 3 Z 9 : 1 4 F 2 2 5 7 7 8 - - - - - Z11:16A1 + Z9:14A1 ( 1 6 : 1 ) 3 7 5 7 1 0 0 - - - - - C E W 4 ( a ) - 1 7 2 2 0 2 0 1 0 2 9 1 2 C E W 3 ( b ) ------2 2 2 0 Z11.16A1 + 16A1 ( 9 0 : 1 0 ) - - - 2 5 3 3 2 5 - - Z11: +Z7:16AI ( 9 9 : 1 ) - - - 1 4 0 2 5 - - Z11: +Z9:16A1 ( 9 8 : 2 ) ------5 0 2 2

(a) = Z11-Z9-Z7-16A (93-2-2-4) - Hexadecenals. (b) = Z11-Z9-Z7- (97-2-1)-Hexadecenals. a . Recovery of tethered females from 70 to 100%.

3 1 5 Table 5. Percent of 10 tethered virgin female H. MI that mated In a 225 m2 plot treated with pharomonal oomponanta evaporated from 38 stations in a 6 x 6 grid (50 hollow flbers/station).

T r e a t m e n t D a y (R a t i o ) 1 2 3 4 13 20

C o n t r o l 7 7 . 8 100 50 5 5 . 5 50 4 0 Z 1 1 : 1 6 A 1 0 0 0 0 0 0 Z11 :16A1 +Z9:14A1 ( 1 6 : 1 ) 0 0 1 1 . 1 0 0 0

and therefore other heliothids is the reliability of the The fortunes of air permeation as a control formulation and delivery system. The original quan• approach are less clear. The method appears more tified studies of air permeation established that dis• feasible with increased technological input. It has ruption of mating is obtained when the amount of not yet been demonstrated that disruption of sex chemical evaporated remains above some critical pheromone communication can be used to protect value per unit area and that the effect is quickly lost a crop from Heliothis damage. The marked reduc• with lesser amounts (Shorey et al. 1972; McLaugh• tion in S. frugiperda oviposition observed during lin et al. 1972). Moreover, male mate-seeking simultaneous trials with H. zea (Mitchell and behavior is apparently not reduced (Farkas et al. McLaughlin 1982) indicate that a noctuid species 1975, Richerson 1977). Thus, an extremely reliable in corn can be markedly influenced by this system for maintaining the disruptant in the crop approach. Research thus far suggests that formu• environment is essential. lation deficiencies and the movement of mated Teal (unpublished data) has found that decom• females among local crops have hampered efforts position still occurs in even the more advanced to demonstrate efficacy with H. zea. formulations of Heliothis aldehydes. This makes One largely unexplored area is the combination their use problematical, but the recent formulation of host odors with pheromones. H. zea, for example, progress is encouraging. Alternative chemicals, is apparently attracted by volatiles from corn silk with greater stability, such as Z9:14F or olefinic (Cantelo and Jacobson 1979). Semiochemical analogs of Z11:16A1 (Carlson and McLaughlin blends that simulate an attractive stage of host 1982, and unpublished data) have not produced before the host reaches that stage might be used to materials with the potency of Z11: 16A1. more closely estimate the potential mating and/or oviposition pressure from a pest. Such chemicals may help to stabilize pheromone-trap captures, which now vary with the relations of trap to crop an d Conclusions stage of crop. Thus far we have attempted to exploit only the The use of heliothid pheromone traps to monitor most obvious aspects of Heliothis behavior, and adult activity is now feasible; however, as with most have expected these to supply near-total control. other lepidopteran pheromones, the information The impact upon mating now apparently possible required to make good use of trapping data is lack• with air permeation may provide the margin ing. Hopefully, the next generation of trapping stu • required for control when integrated with other dies will concentrate on the parameters necessary measures. Pheromones have not been included to to generate predictive models of insect popula• any extent in integrated control research projects. tions. The formulation of pheromonal components We have not yet explored the behavioral depths of for use in traps is still in a state of flux; however, species' communication in Heiothis. Mate-finding, these problems should be more easily overcome host-finding, and the basic process of olfaction are than those involved in the development of formula• critical to any organism's survival and, as such, tions for disruption. vulnerable to our manipulation.

3 1 6 References MCLAUGHIN. J.R., SHOREY, H.H., GASTONI, L.K., KAAE, R.S., and STEWART, F.D., 1972. Sex pheromones of Lepidoptera. XXXI. Disruption of sex phero m o n e

BEROZA, M. 1976. Control of the gypsy moth and other communication in Pectinophora gossypiella with hexa- insects with behavior-controlling chemicals. Pages 9 9 - lure. Environmental Entomology 1:645-650.

118 in Pest management with insect attractants, ed. Mor• MCLAUGHLIN, J.R., MITCHELL, E.R., and CROSS, ton Beroza. American Chemical Symposium Series 23, J . H . 1981 Field and laboratory evaluation of mating dis- Washington, DC, USA. ruptants of Heliothis zea a n d Spodoptera frugiperda in Florida. Pages 243-251 in Management of insects with CANTELO, W.W., and JACOBSON, M. 1979. C o r n silk semiochemicals, ed. E.R. Mitchell. New York, USA:Pl e - volatiles attract many pest species of moths. Journ a l of n u m Press. Environmental Science and Health A14.695-707. MITCHELL, E.R., JACOBSON, M., and BAUM- C A R D E T . 1 9 8 1 . Disruption of long-distance phero- HOVER, A.H. 1975. Heliothis spp.: Disruption of phe- mone communication in the Oriental fruit moth: camo u • romonal communication with (Z)-9-tetradecen-1-ol flaging the natural aerial trials from females? Pag e s formate. Environmental Entomology 4:577-579. 3 8 5 - 3 9 8 in Management of insect pests with semiochemicals, ed. E.R. Mitchell. New York, USA: Plenum Press. MITCHELL, E.R., BAUMHOVER, A.H. and JACOB- SON, M. 1976. Reduction of mating potential of male CARLSON, D.A., and MCLAUGHLIN, J.R. 1982. D i o - Heliothis spp. a n d Spodoptera frugiperda in field plots lefin analog of a sex pheromone component of Heliothis treated with disruptants. Environmental Entomology zea active in disrupting mating communication. Experie n - 5 : 4 8 4 - 4 8 6 . tia (in press). MITCHELL, E.R., and McLAUGHLIN, J.R. 1982. S u p • FARKAS, S.R., SHOREY, H.H., and GASTON, L.R. pression of mating and oviposition by fall armyworm a n d 1975. Sex pheromones of Lepidoptera. The influence of mating by corn earworm in corn using the air permea t i o n prolonged exposure to pheromone on the behavior of technique. Journal of Econonomic Entomology (in press). m a l e s of Trichoplusia ni. Environmental Entomology 4 : 7 3 7 - 7 4 1 . PRIMIANI, N.M. 1979. Ethological significance of com• pounds comprising the female sex pheromone of Helio• GASTON, L.K., SHOREY, H.H., and SAARIO, C.A. this zea a n d Heliothis virescens. Ph.D. Dissertation, 1967. Insect population control by the use of sex phero• University of Maryland , Md, USA. 110 pp. mones to inhibit orientation between the sexes. Nat u r e 2 1 3 : 1 1 5 5 . RICHERSON J.V. 1977. Pheromone-mediated behav• ior of the gypsy moth. Journal of Chemical Ecology 3:291 - KEHAT, M., GOTHILF, S., DUNKELBLUM, E., and 3 0 8 . GREENBERG, S. 1980. Field evaluation of female sex pheromone components of the cotton bollworm, Heliothis ROELOFS, W.L. 1978. Threshold hypothesis for phero• armigera, Entomologia Experimentalis et Applicata mone perception. Journal of Chemical Ecology 6:685- 7 : 1 8 8 - 1 9 3 . 6 9 9 .

KLUN, J.A., CHAPMAN, O.L., MATTES, K.C., WOJT- ROTHSCHILD, G.H.L. 1978. Attractants for Heliothis KOWSKI, P.W., BEROZA, M., and SONNET P.E. armigera a n d H. punctigera. Journal of Australian Ento• 1 9 7 3 . Insect sex pheromones: minor amount of opposite mology 102:389-390. geometrical isomer critical to attraction. Science SHOREY, H.H., GASTON, L.K., and SAARIO, C.A. 181:661-663. 1967. Sex pheromones of noctuid moths. XIV. Feasibility KLUN, J.A., CHAPMAN, O.L., MATTES, K.C., and of behavioral control by disrupting pheromone commu n i • BEROZA, M. 1975. European corn borer and redbanded cation in cabbage loopers. Journal of Economic Ento m o l • leafroller: Disruption of reproduction behavior. En v i r o n • ogy 60:1541-1545. mental Entomology 4:871 -876. SHOREY, H.H., KAAE, R.S., GASTON, L.K., and KLUN, J.A., PLIMMER, J.R., BIERL-LEONHARDT, MCLAUGHLIN, J.R. 1972. Sex pheromones of Lepidop• B.A., SPARKS, A.N., and CHAPMAN, O.L. tera. XXX. Disruption of sex pheromone communicatio n in 1 9 7 9 . Trace chemicals: The essence of sexual com• Trichoplusia ni as a possible means of mating control. munication systems in Heliothis species. Science Environmental Entomology 1:641 -645. 204:1328-1330. SHOREY. H.H., GASTON, L.K., and KAAE, R.S. KLUN, J.A., PLIMMER, J.R., BIERL-LEONHARDT, 1976. Air-permeation with gossyplure for control of the B.A., SPARKS, A.N., PRIMIANI, M., CHAPMAN, O.L., pink bollworm. Pages 67-74 in Pest management with LEE, G.H., and LEPONE, G. 1980. Sex pheromone insect sex attractants, ed. Morton Beroza. American chemistry of female corn earworm moth, Heliothis zea Chemical Society Symposium Series 23, Washington, Journal Chemical Ecology 6:165-175. D C , U S A .

3 1 7 SHOREY, H.H. 1977. Manipulation of insect pests of agricultural crops. Pages 353-367 in Chemical control of insect behavior, eds. H.H. Shorey and J.J. McKelvey , Jr. New York, USA: John Wiley.

SILVERSTEIN, R.M. 1981. Pheromones: background and potential for use in insect pest control Science 213:1326-1332.

TEAL, P.E.A., MCLAUGHLIN, J.R., and TUMLINSON, J.H. 1981a. Analysis of the reproductive behavior of Heliothis virescens (F.) under laboratory conditions. Annals of the Entomological Society of America 74:3 2 4 - 3 3 0 .

TEAL, P.E.A., HEATH, R.R., TUMLINSON J.H., and MCLAUGHLIN, J.R. 1981b. Identification of a sex p h e r o m o n e of Heliothis subllexa (Gn.) (Lepidoptera: Noc- tuidae) and field trapping studies using different b l e n d s o f components. Journal of Chemical Ecology 7:1011 -102 2 .

TINGLE, F.C., and MITCHELL, E.R. 1981. R e l a t i o n - ships between pheromone trap catches of male tobacc o budworm, larval infestations, and damage levels in tobacco. Journal of Economic Entmology 74.437-440.

TUMLINSON, J.H., HENDRICKS, D.E., MITCHELL, E.R., DOOLITTLE, R.E., and BRENNAN, M.M. 1 9 7 5 . Isolation, identification, and synthesis of the se x pheromone of the tobacco budworm. Journal of Chemic a l Ecology 1:203-324.

3 1 8 Preliminary Studies on the Female Sex Pheromones of Heliothis Species and Their Possible Use in Control Programs in Australia

G.H.L. Rothschild, A.G.L. Wilson, and K.W. Malafant*

Abstract

The role of pheromone traps in scouting for H e l i o t h i s spp was examined in cotton crops in eastern Australia. A 50:50:1 mixture of (Z)-11-hexadecenal, (Z)-11-hexadecenyl acetate, and (Z)-9-tetradecenal was a specific attractant for H. punctigera. Males of H. armigera were captured at baits containing a 10:1 mixture ot(Z)-11-hexadecenal, and (Z)-9-hexadecenal, but significant numbers of H. punctigera were also taken when this species was abundant. A comparison was made between adult captures at pheromone (and light) traps and egg counts in the crop. Analyses of the data, using a linear model, indicated that 85% of the deviance in the relationship between egg counts and pheromone-trap catches could be accounted for by the regression, while the corresponding figure for light-trap captures and egg counts was 78%. There was also a significant positive relationship between pheromone-trap captures and temperatures during the daily flight period, and some additional evidence for interactions with wind speed and direction. Although there was a highly significant correlation between pheromone-trap captures and egg counts, it appeared that the confidence limits for predicting egg numbers from catch data may have been unacceptably large in practical terms; decisions to spray are often based on relatively low egg counts. The use of pheromones for mating disruption of Heliothis spp in Australia is being considered, but the level of work in this area will depend on the outcome of studies on the suitability of these insects for such a control strategy. Limiting factors may include local dispersal or long-distance migration of mated females.

*Commonwealth Scientific and Industrial Research Organisation (CSIRO); respectively: Division ot Entomology, Canberra, ACT; Division of Plant Industry, Narrabri, NSW; and Division of Mathematics and Statistics, Canberra, ACT, Australia.

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, AP., India. 3 1 9 L'utilisation de pheromones dans le but de causer une confusion lors de I'accouplement d ' H e l i o t h i s spp en Australie est envisagee, mais le travail dans ce domaine dependra des resultats des e t u d e s sur la r6ponse de ces insectes a une telle strategie de lutte. Les fac- teurs limitants peuvent etre une dispersion locale ou une migration sur de tongues distances des temelles accouplees.

Two species of Heliothis are of particular impor• Z11 -16;ALD alone, although baits with this single tance as pests of crops in Australia: H. punctigera c o m p o n e n t have b e e n used e l s e w h e r e i n c o m m e r • W a l l e n g r e n , a species native to Australia a n d adja• cially available monitoring kits, with variable results cent islands, and the well-known H. armigera (Bourdouxhe 1980). Only small numbers of H. (Hubner), which is widely distributed throughout punctigera males w e r e taken in traps baited with t h e O l d W o r l d . the aldehydes, but catches were greatly increased The sex pheromones of Heliothis h a v e recently by the addition of (Z)11 - h e x a d e c e n y l acetate (Z11 - become the subject of investigation in Australia, 16;Ac). and significant progress in the development of spe• T h e p r e s e n c e of Z11 -16:ALD in female H. armig• cific attractants for the two major species has been era was confirmed by Piccardi et al. (1977), who made in the past 2 years. This report describes the attributed the poor results of their field tests to low current status of work on the identification of the moth populations. As noted a b o v e , a more likely components of the female sex pheromone blends, explanation was that the aldehyde was not particu• a n d d i s c u s s e s attempts to use these materials as larly attractive in the absence of other components trap baits to monitor the activity and abundance of present in the natural blend. This was confirmed by Heliothis species. The study was prompted by the work of Nesbitt et al. (1979, 1980), which requests from government and commercial agen• i n c l u d e d joint field trials with the CSIRO Division of cies involved in s c o u t i n g for Heliothis infestations, Entomology. The most important minor component particularly in cotton. Most scouting methods are of H. armigera females w a s s h o w n to be ( Z ) - 9 - b a s e d on e g g c o u n t s , but it is not possible to assign hexadecenal (Z9-16:ALD)—Z9-14:ALD could not eggs or early larval instars to a particular species. It be detected in female extracts or effluvia. The is of s o m e i m p o r t a n c e to k n o w the species c o m p o • increase in c a t c h e s , in traps baited with Z 1 1 - sition of individual crop infestations, as this may 16: ALD, together with up to 10% of Z9-16; ALD, was influence the control strategy used; for example, H. significantly greater than that when Z9-14: ALD was armigera is resistant to a number of insecticides, a d d e d to Z 1 1 - 1 6 : A L D . whereas resistance has not yet been detected in H. T h e identity of the female sex p h e r o m o n e of H. punctigera. punctigera is only partially resolved, but work so far indicates that the major components are Z11- 16:ALD, Z11 -16:Ac and (Z)-11 -hexadecenol (Z11- 16:OH) with s o m e e v i d e n c e for t h e p r e s e n c e of Pheromone Blends of H. armigera (Z)-7-hexadecenal (Z7-16.ALD) and hexadecanal and H. punctigera (16:ALD) (Rothschild et al. 1982). In the field, H. punctigera males are c a p t u r e d in significant The search for attractants for H. armigera a n d H. numbers with mixtures of equal parts of Z11- punctigera b e g a n in 1975, with the s c r e e n i n g of 16:ALD a n d Z 1 1 - 1 6 : A c , but only if 1 to 1 0 % of c o m p o u n d s k n o w n at that time to be c o m p o n e n t s Z9-14:ALD is also included. So far, however, it has of the sex pheromones of New World species of not b e e n possible to detect t h e last c o m p o u n d in Heliothis, H. zea a n d H. virescens: ( Z ) - 1 1 - t h e female. hexadecenal (Z11-16.ALD) and (Z)-9- At present, monitoring of Heliothis species in tetradecenal (Z9-14:ALD) (Roelofs et al. 1974; Australia is b a s e d on a 50:50:1 mixture ( Z 1 1 - Tumlinson et al. 1975). These trials (Rothschild 16:ALD:Z11-16:Ac:Z9-14:ALD) for H. punctigera, 1978) indicated that H. armigera w a s attracted to a n d a 10:1 mixture of Z11 - 1 6 : A LD a n d Z 9 - 1 6 : A L D mixtures of the aldehydes, with the greatest for H. armigera. T h e H.punctigera traps are highly catches at traps baited with mixtures of the two specific—of 15990 males captured in ten localities compounds containing less than 10% of the Z9- in 1 9 7 8 - 1 9 8 0 , only 46 w e r e H. armigera (0.3%); 14;ALD. Relatively few males were attracted to similar levels of H. armigera m a l e s w e r e r e c o r d e d

3 2 0 in blank traps. Considerable "contamination" (< males at pheromone-baited traps with numbers of 20%) of H. armigera catches by H. punctigera males and females taken in light traps, and males w a s noted w h e n Z 9 - 1 4 : A L D w a s used in the numbers of eggs laid in the c r o p — t h e latter being baits, but this w a s r e d u c e d to an average of 6% the main criterion used by scouting agencies w h e n w h e n the c o m p o u n d was replaced by Z 9 - 1 6 : A L D , making decisions on the necessity for applying the naturally occurring minor component. How• chemical control measures. The results discussed ever, unacceptably high levels of "contamination" here relate to only two seasons, in the s e c o n d of are still being recorded in the season, particualrly in w h i c h Heliothis numbers, in terms of crop infesta• Queensland, and further work is required to tions, were particularly low. However, more exten• increase the specificity of the H. armigera bait. sive studies are now being undertaken in a wide range of crops by entomologists in three Australian States, using pheromone baits from the same Pheromone Dispensers and Traps source, the CSIRO Division of Entomology.

Many types of dispensers have been used as sub• strates for Heliothis pheromones, ranging from Field Tests—Namoi Valley, 1978-80 filter-paper wicks (Tumlinson et al. 1975) to PVC During the 1978-79 season, Heliothis activity was laminates (Hendricks and Hartstack 1978). In the monitored in cotton crops in nine sites located Australian trials, small pieces of red rubber tubing along about a 60-km east-west transect in the were used (Rothschild 1978), impregnated with lower Namoi Valley (New South Wales). Three H. 500 µg of Z11 -16:ALD (plus c o r r e s p o n d i n g q u a n • armigera and three H. punctigera traps were tities of the other components), together with an placed immediately adjacent to the crop at each equal quantity of an antioxidant (BHT-2,6-di-tert- site. A mercury-vapor light trap was also located in butyl-p-cresol), were effective for at least 2 weeks one of the sites. At this particular locality, captures under the hottest summer conditions (day temper- from the light traps a n d the p h e r o m o n e traps were atures>40°C). r e m o v e d daily for 4 successive days e a c h week, Many types of traps have been devised for trap• followed by one collection after the remaining 3 ping Heliothis species, particularly in the USA. days. The numbers of eggs on plants in six ran• T r a p s used in preliminary s c r e e n i n g trials in A u s • domly selected 1 -m rows were also recorded on tralia relied on a d h e s i v e - c o v e r e d liners to retain the same occasions. White eggs (<24 hours old) captures, and have been described elsewhere were scored separately from older brown eggs. In (Rothschild 1978). Water traps, which are more the remaining sites, captures at pheromone traps efficient than adhesive-lined ones, were used in the a n d egg counts were obtained twice weekly. Identi• monitoring trials discussed in this report: these cal H. punctigera baits were used in 1978-79 a n d consisted of a plastic tray (35 x 30 x 10 cm) con• 1979-80, but Z9-16:ALD replaced Z9-14:ALD in taining 2 liters of water plus a little detergent. Th e the H. armigera blend in the s e c o n d season, follow• tray was located on a w o o d e n support, a n d pro• ing the identification of the former c o m p o u n d in tected by a wooden cover from which the bait was female effluvia in that year (Nesbitt et al. 1979, suspended. In more recent trials these trays have 1980). been replaced by dry funnel traps of the type des• Trapping results and egg counts for two sea• cribed by Kehat and Greenberg (1978), as these sons, from the site at w h i c h sampling was most are easier to maintain. In most monitoring trials, regular, are shown in Figures 1 a n d 2. Analysis of traps have been located immediately adjacent to data from the remaining sites is still incomplete, the crop (preferably between blocks), at just above and only general comments can therefore be made c r o p height a n d at a spacing of 20 to 50 m. about capture patterns between localities.

Monitoring Activity of Species Composition of Catches Heliothis Species H. punctigera was the dominant species in both T h e objectives of the limited monitoring trials so far pheromone- and light-trap catches, but there was undertaken have b e e n to c o m p a r e the captures of little c o r r e s p o n d e n c e between c a t c h e s in the t w o

321 A

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2 0

D e c J a n Feb Mar

B 8 2 4 H. punctigera 8 0 0 30 H. armigera

Egg counts

4 0 0

e g g s / m

1 0 0 8 0

D e c J a n Feb M a r

Figure 1. A. Male Heliothis adults captured at pheromone traps, Myall Vale, 1978-79. SQ, FL: Square and flower formation In cotton crop. B. Heliothis adults (both sexes) captured at a light trap, and egg counts per meter row of cotton. Myall Vale, 1978-79.

3 2 2 SQ FL A 6 7 52 45 44 40

2 . 0

30 1.0

e g g / m

10-

N o v D e c J a n Feb Mar

409 196 B 2 0 5 202 H. punctigera 160 H. armigera

Egg counts

8 0

4 0

N o v D e c Jan Feb Mar

Figure 2. A. Male Heliothis adults captured at pheromone traps and egg counts per meter row of cotton, Myall Vale, 1979-80. SQ, FL: Square and flower formation in cotton crop. B. Heliothis adults (both sexes) captured at a light trap, Myall Vale, 1979-80.

3 2 3 monitoring devices, regardless of whether male or between numbers of adults (males) captured in f e m a l e captures in light traps w e r e being c o n s i • p h e r o m o n e traps a n d e g g s laid in the crop. dered. Comparisons of the relative numbers of Although the relationship b e t w e e n egg c o u n t s e a c h species taken in p h e r o m o n e traps in 1979-80 and pheromone-trap captures in 1978-79 was sta• w e r e probably more meaningful t h a n those m a d e in tistically significant, it may not prove possible, on 1978-79, as a more effective bait for H. armigera the basis of these data, to predict e g g numbers in w a s used in t h e s e c o n d season. T h e r e w a s insuffi• the c r o p from m o t h captures with sufficient a c c u • cient information from larval rearing to compare racy to be of practical value. A figure of 5 eggs/ m of trapping figures for each species with species row (or m2 of crop) has been cited as a threshold c o m p o s i t i o n o f l a r v a e i n f e s t i n g t h e c r o p . density in the Namoi Valley, above which chemical Pheromone-trap captures in crops such as wheat control measures may be required (Room 1979). In a n d maize, w h i c h are hosts of H. armigera, but the present analysis, a density of >5 eggs/m was rarely H. punctigera (Wardhaugh et al. 1980), associated with mean pheromone-trap captures included a much greater proportion of the former (both species)/trap per night that ranged (in terms species (42%) than captures in cotton (12%). of extreme values) from 2.3 to 53.7. For egg counts of <5 eggs/m, the corresponding captures ranged from 0 to 53.3. It will be n e c e s s a r y to test the Prediction of Egg Counts from Trap Captures practicality of the confidence limits of this relation• ship under field conditions. As noted earlier, it is not possible to distinguish In the 1 9 7 9 - 8 0 season, w h e n egg n u m b e r s rarely b e t w e e n t h e eggs of the t w o Heliothis species, and exceeded 1 per m (Fig. 2), less than 50% of the comparisons of egg numbers with catches at light d e v i a n c e in the relationship b e t w e e n egg c o u n t s traps a n d p h e r o m o n e traps were therefore b a s e d and pheromone traps (or light traps) could be on pooled c o u n t s of H. armigera a n d H. punctigera. accounted for by the regression. T h e d a t a in Figure 1 indicate that there is a general Failure to obtain sufficient daily data for analysis relationship b e t w e e n egg counts a n d p h e r o m o n e - may have been responsible for the imprecision of trap catches, and, to a lesser extent, light-trap cap• t h e r e l a t i o n s h i p b e t w e e n e g g c o u n t s a n d tures in 1978-79, when the infestation level (in pheromone-trap captures, but it is equally probable terms of oviposition in the crop) was high; in the that at least some of the variability arises from the following s e a s o n , w h e n the infestation was m u c h effects of the many factors that influence both ovi• lower (Figure 2), there was no apparent relationship position in the c r o p a n d the c a p t u r e rate of Heliothis b e t w e e n trap c a p t u r e s a n d e g g counts. males at pheromone traps. These could include the T h e 1 9 7 8 - 7 9 data were analyzed using a linear sudden influx of migrants, particularly mated and m o d e l , w h i c h related the total e g g count for a day to unmated females; the former would provide a sud• the pheromone- or light-trap catch for that day, and d e n boost to egg numbers, a n d t h e latter might environmental factors such as temperature and divert males away from pheromone traps. Dramatic w i n d s p e e d a n d direction. A log s c a l e w a s u s e d for increases in daily egg counts without any compar• both the e g g c o u n t s a n d trap c a t c h e s . Only white able c h a n g e in p h e r o m o n e trap captures were eggs were considered in the analysis of data noted in s o m e of the N a m o i Valley sampling sites, derived from daily counts, as such eggs were less particularly early in the season; these increases t h a n 24 hours old. were largely attributed to H. punctigera (A.G.L. Wil• T h e analysis indicated that 8 5 % of the d e v i a n c e son, unpublished data). in the relationship b e t w e e n e g g c o u n t s a n d T h e influence of the type of c r o p a n d flowering pheromone-trap catches could be accounted for pattern on the relationship b e t w e e n trap captures by the regression, while the c o r r e s p o n d i n g figure and egg counts is not clear. Flowering crops are for the relationship between light-trap captures and particularly attractive to ovipositing Heliothis egg counts was 78%. Analysis of egg counts on a females, a n d the flowering period may range from 7 given day a n d p h e r o m o n e trap c a t c h e s on the to 14 days in sunflowers to over 50 for lucerne a n d same or each of the previous 7 days, indicated that over 120 days for cotton (Wardhaugh et al. 1980). data collected on the s a m e day p r o d u c e d the high- Recent comparisons of egg counts and est correlation of 0.60, d e c r e a s i n g to 0.48 a n d 0.10 pheromone-trap captures (3-day totals prior to egg by d a y s 5 a n d 7 respectively. T h e r e is thus no counts) in Queensland produced statistically sig- evidence of a 'lag' effect in the relationship nificant positive correlations in lucerne a n d s u n -

3 2 4 flowers but not in cotton or s o y b e a n s (B. Pyke, tures at light traps in the Namoi Valley has been Department of Entomology, University of Q u e e n s • very fully analyzed by Morton et al. (1981). land, personal communication).

Other Factors Affecting Catch Effect of Weather on Pheromone-Trap Catches The effects of other environmental factors such as m o o n l i g h t a n d b a r o m e t r i c p r e s s u r e o n pheromone-trap captures have not yet been e x a m • The linear regression model referred to above was ined in Australia, although the raw data have n o w e m p l o y e d to e x a m i n e the relationship b e t w e e n e g g been collected. Moonlight and air pressure are said counts a n d trap c a t c h e s , a n d to determine whether to influence captures of Heliothis spp in the USA this was further influenced by certain environmen• (Hendricks and Hartstack 1978; Hartstack et al. tal variables. As discussed earlier, the regression 1978). Other information still to be analyzed a c c o u n t e d for m u c h of the deviance, but there was includes the influence of pesticide treatments on also s o m e evidence of an interaction with w i nd captures at pheromone traps in Namoi Valley cot• speed (significant at P<0.1 but not <0.05). T h e direct ton crops. effects of temperature (daily average, maximum, m i n i m u m , and 2-hourly records during the daily flight period) a n d w i n d speed a n d direction (4- hourly records) on trap captures were examined. Trap Captures and Heliothis Phenology Rainfall (and irrigation) was not included in the analysis as this was recorded on relatively few of T h e trap captures s h o w n in Figures 1 and 2 do not the sampling occasions. reveal any distinct flight periods that could be T h e analysis indicated that average or m i n i m u m attributed to successive generations. To reveal daily temperature accounted for 84% of the s u c h trends, it may be necessary to adjust c a t c h e s d e v i a n c e in the regression with p h e r o m o n e - t r a p in terms of environment variables in the manne r captures. T h e r e was also e v i d e n c e of an interac• suggested by Morton et al. 1 9 8 1 . Even after they tion with both wind speed and direction, but this was had m a d e s u c h adjustments to light-trap captures, significant only at P < 0 . 1 and not < 0.05; c a t c h e s these workers were unable to distinguish distinct d e c r e a s e d with increasing w i n d s p e e d a n d m o r e generations for H. punctigera; in this species there moths w e r e captured w h e n traps w e r e d o w n w i n d was presumably constant recruitment into cotton of the crop. It c o u l d be e x p e c t e d that the two latter of individuals from a succession of other host parameters would influence pheromone-trap per• plants. T h e r e was, however, e v i d e n c e of three dis• f o r m a n c e as captures w o u l d be in part d e p e n d e n t tinct periods of a b u n d a n c e of H. armigera, with this on the n u m b e r s of Heliothis males flying upwin d in species replacing H. punctigera from midsummer response to windbome odor cues. Temperature (late December) onwards. This pattern was not would influence both the level of flight activity of the evident in the present trials where H. punctigera males a n d the release rate of p h e r o m o n e c o m p o • appeared to predominate until late February, in nents from the trap baits. There was no evidence of both seasons (Figure 1 a n d 2). a lower temperature threshold for captures at pheromone traps; this threshold is therefore pre• sumably below 10°C, the lowest temperature The Use of Monitoring Traps recorded during the daily flight period in the cotton in Control Programs c r o p in 1 9 7 8 - 7 9 or 1979-80. At light traps, captures of both Heliothis species ceased at approximately No attempts have yet been m a d e to use p h e r o • 13°C. The daily average or minimum temperatures mone traps as a basis for planning chemical con• a c c o u n t e d for about 9 0 % of the d e v i a n c e of the trol measures in Australia. At this stage, regression with light-trap catch. There was evi• experimental results suggest that traps (1) indicate d e n c e of an interaction with w i nd s p e e d but not w h e n moths first invade a crop, (2) provide c r u d e direction. Wind speed presumably affected flight information on probable oviposition levels (e.g. activity, but there w a s no directional effect as the high, m e d i u m , or low), and (3) give an indication as light trap w a s open on all sides. T h e influence of to w h i c h Heliothis species is present. Although these environmental variables on Heliothis c a p - further work relating population levels in the crop to

3 2 5 adult trap captures is clearly necessary, prelimi• likely efficacy of mating disruption in Heliothis c o n • nary trials are to be undertaken to compare Helio• trol in Australia. One critical question is whether this control in fields where chemical treatments are mated females of H. armigera a n d H. punctigera based on egg counts alone, capture thresholds at are involved in long-distance migration or local pheromone traps alone, or a combination of the two dispersal. The extent to which such movements measures of abundance. occur will have an important bearing on the out• In the USA, pheromone-trap captures have been come of mating disruption effected by the phero• incorporated into predictive models designed to mone treatment. This question will be examined provide information on probable oviposition pat• before extensive work with potential disruptants is terns and population abundance of Heliothis spp undertaken. in cotton crops (Hendricks and Hartstack 1978; Hartstack et al. 1978). Results so far suggest that the traps may provide a 2- to 4-day warning of Acknowledgments significant increases in crop infestation early in the season, but that, later, there is a "drift" and peak Considerable assistance with many aspects of the captures may occur 3 or 4 days before or after peak field and laboratory work was provided by Mr. R.A. egg laying. Vickers and Mr. S. Bakker (CSIRO Division of Ento• mology) and Mr. L. Bauer (CSIRO Division of Plant Industry). Mating Disruption

No research has so far been undertaken in Austra• lia to investigate the possibility of using synthetic References pheromones or other behavior-modifying com• p o u n d s for Heliothis control through mating disrup• B O U R D O U X H E , L. 1 9 8 0 . S t u d y of c h a n g e s in Heliothis tion. It is planned to begin research on this problem armigera flights with synthetic pheromone traps in Sene• in the 1981 -82 field season in cotton. All that has gal. F A O Plant P r o t e c t i o n Bulletin 2 8 : 1 0 7 - 1 0 9 . been done so far is to combine standard monitoring G O T H I L F , S., K E H A T , M . , J A C O B S O N , M . , and baits for H. punctigera a n d H. armigera with various G A L U N , R . 1978. Screening pheromone analogues by compounds to see whether catches are reduced. EAG technique for biological activity on males of Earias Compounds tested in amounts of 10 000 and 1000 insulana, Heliothis armigera, a n d Spodoptera littoralis. ug have included (Z)-9-tetradecenyl formate (Z9- Environmental Entomology 7:31 -35. 14:Fo), a pheromone "mimic" of Z11-16:ALD H A R T S T A C K , A . W . , H O L L I N G S W O R T H , J . P . , known to disrupt mating of Heliothis spp in the USA W I R T Z , J.A., B U C K , D.R., L O P E Z , J . D . , and H E N • (Mitchell et al. 1976), and (E) and (Z)-9- D R I C K S , D . E . 1978. Relation o f t o b a c c o b u d w o r m tetradecenyl acetate (Z9-14:Ac). There was no sig• c a t c h e s i n p h e r o m o n e b a i t e d t r a p s t o field populations. nificant reduction in captures of H. punctigera or H. Southwestern Entomologist 3:43-51. armigera in any of the treatments in tests over a H E N D R I C K S , D . E . , a n d H A R T S T A C K , A . W . 34-day period. Gothilf et al. (1978), however, have 1978. Pheromone trapping as an index for initiating con• shown that captures of H. armigera are reduced by trol of c o t t o n insects, Heliothis spp: a c o m p e n d i u m . Pro• over 95% when septa loaded with 1000 ug of Z9- ceedings, 1978 Beltwide Cotton Research Conference.

14:Fo or Z9-14z;Ac are placed adjacent to virgin K E H A T , M . , and G R E E N B E R G , S . 1 9 7 8 . Efficiency of females of this species. Possible reasons for the t h e s y n t h e t i c sex attractant a n d t h e effect of trap size on difference between the results of tests with virgin captures of Spodoptera littoralis males in water traps and females and synthetic pheromone sources include in dry funnel traps. Phytoparasitica 6:79-83. (1) inhibition of female "calling" by the added com • M I T C H E L L , E.R., B A U M H O V E R , A . H . , and J A C O B - pounds, or (2) the inability of males to perceive the S O N , M . 1 9 7 6 . R e d u c t i o n o f m a t i n g potential o f m a l e female signal in the presence of these compounds, Heliothis s p p . a n d Spodoptera trugiperda in field plots because the release rate and composition of the treated with disruptants. Environmental Entomology pheromone blend from the virgin female may differ 5 : 4 8 4 - 4 8 6 . significantly from that produced from the synthetic M O R T O N , R., T U A R T , L.D., and W A R D H A U G H , K . G . pheromone source. 1 9 8 1 . T h e a n a l y s i s a n d s t a n d a r d i s a t i o n o f light-trap At this stage it is possible to only speculate on the c a t c h e s of Heliothis armiger (Hubner) and H. punctiger

326 Wallengren (Lepidoptera:Noctuidae). Bulletin of Ent o m o • logical Research 71:207-225.

NESBITT, B.F., BEEVOR, P.S., HALL, D.R., and LES• TER, R. 1979. Female sex pheromone components of the cotton bollworm Heliothis armigera. Journal of Insect Physiology 25:535-541.

NESBITT, B.F., BEEVOR, P.S., HALL, DR., and LES• TER, R. 1980. (Z)-9-Hexadecenal: a minor component of the female sex pheromone of Heliothis armigera (Hubner) (Lepidoptera:Noctuidae). Entomologia Experi- mentalis et Applicata 27:306-308.

PICCARDI, P., CAPIZZI, A., CASSANI, G., SPINELLI, P., ARSURA, E., and MASSARDO, P. 1977. A sex pheromone component of the old world bollworm Helio• this armigera. Journal of Insect Physiology 23:1443-1445.

ROELOFS, W.L., HILL, A,.S., CARDE, R.T., and BAKER, T.C. 1974. Two sex pheromone components of the tobacco budworm moth, Heliothis virescens. Life Sciences 14:1555-1562.

ROOM, P.M. 1979. A prototype 'on-line' system for man• agement of cotton pests in the Namoi Valley, New So u t h Wales Protection Ecology 1:245-264.

ROTHSCHILD, G.H.L. 1978. Attractants for Heliothis armigera a n d H. punctigera. Journal of the Australian Entomological Society 17:389-390.

ROTHSCHILD, G.H.L., NESBITT, B.F., BEEVOR, PS., CORK, A., HALL, D.R., and VICKERS, R.A. 1982. Studies of the female sex pheromone of the native b u d w o r m , Heliothis punctiger Wallengren. Entomologia Experimentalis et Applicata 31 (in press).

TUMLINSON, J.H., HENDRICKS, D.E., MITCHELL, E.R., DOOLITTLE, R.E., and BRENNAN, M.M. 1975. Isolation, identification, and synthesis of the se x pheromone of the tobacco budworm. Journal of Chemic a l Ecology 1:203-214.

WARDHAUGH, K.G., ROOM, P.M., and GREENUP, L.R. 1980. The incidence of Heliothis armigera ( H u b n e r ) a n d H. punctigera Wallengren (Lepidoptera: Noctuidae) on cotton and other host-plants in the Namoi valley of New South Wales. Bulletin of Entomological Research , 70:113-131.

327

The Potential for Hybrid Sterility in Heliothis Management

F.I. Proshold, M.L. Laster, D.F. Martin, and E.G. King*

Abstract

The discovery of inherited backcross male sterility as a result of hybridization has stimulated interest in controlling field populations of tobacco budworms, H e l i o t h i s virescens (F.), by releasing backcross insects. In 1977, a pilot test was initiated on St. Croix, U.S. Virgin Islands, to test the feasibility of this technique in an isolated ecosystem. Released males did not disperse tar from release sites. The released females were active earlier in the evening than native insects, but mating interaction between released and native occurred at random when backcross pupae were placed in field cages and allowed to emerge and disperse. Further, by release of backcross insects, sterility was infused into native males in great enough numbers to prevent population buildup. This frequency of backcross insects increased as long as releases continued. Over 10 million backcross and H. virescens pupae were reared by the Bioenvironmental Insect Control Laboratory, Agricultural Research Service, U.S. Department of Agriculture, Stoneville, Mississippi, tor conduct of this pilot test during 1977-1980. During the period mid-August to mid-December 1980, over 5 million backcross pupae were shipped to St. Croix for release of about 40 thousand moths per day.

Literature Review d u c e d without altering the mating behavior or abil• ity to disperse a n d find mates in nature. T h e s e Knipling (1960) e x p r e s s e d the view that strains of strains c o u l d be released to control populations in a insects with lethal characteristics might be pro- manner similar to that of males sterilized by radia• tion. In 1972, Laster reported the successful *U.S. Department of Agriculture, Agricultural Research Service; hybridization of Heliothis subflexa ( G u e n e e ) a n d H. respectively: Virgin Islands Experiment Station, St. Croix. U.S. virescens (F.), (Laster 1972). T h e hybrid m a l e s Virgin Islands; Delta Branch Experiment Station, Stoneville, Mis- were sterile, but hybrid females r e p r o d u c e d w h e n sissippi; and Bioenvironmental Insect Control Laboratory, Stone- ville, Miss., USA. crossed with H. virescens males. Further, s o n s of

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India. 329 the hybrid females were sterile, but daughters were s p e r m to the female's s p e r m a t h e c a w a s also res• fertile w h e n c r o s s e d with H. virescens males. This tored, as was his fertility (Proshold and LaChance inherited backcross male sterility persisted through 1974; K a r p e n k o a n d Proshold 1977). If H. subflexa

more than 100 subsequent generations. Laster w a s the P1 female, normal eupyrene sperm transfer s u g g e s t e d that the hybrid males from the H. sub- a n d fertility w e r e restored only w h e n hybrid a n d llexa f e m a l e x H. virescens male c r o s s be released backcross females were crossed with H. subflexa to control populations of H. virescens. T h e differen- males. When these hybrid and backcross females tial in size a n d d e v e l o p m e n t a l time b e t w e e n the w e r e c r o s s e d with H. virescens males, inherited sexes was proposed as a means of obtaining only b a c k c r o s s male sterility persisted for more than 90 males for release. Subsequently, Knipling and generations (Martin et al. 1981a). Klassen (1976) a n d Laster et al. (1976) presented In o n e study, hybrid females (H. subflexa female models that demonstrated the powerful suppres• x H. virescens male) and backcross females were sive potential or releasing hybrid a n d / o r b a c k c r o s s c r o s s e d with H. virescens males for 35 g e n e r a • females as well as males, so that the sterile-male tions. Chromosome pairing in spermatocytes of trait w o u l d be introduced into the native population. BC35 males exhibited no nonhomology. T h e n BC35 M a k e l a a n d Huettel (1978) refined a n d e x p a n d e d females were crossed with H. subflexa males. t h e s e models. T h e powerful potential of this Spermatocytes of progeny from this cross exhi• method of control stimulated considerable bited the s a m e types of desynapsis as observed in

r e s e a r c h along t w o lines: (1) to determine the F 1 hybrid males. Females m a t e d to these males behavior a n d competitive ability of the b a c k c r o s s failed to receive e u p y r e n e sperm in their sper• insect in c o m p a r i s o n with pure H. virescens; a n d m a t h e c a a n d w e r e sterile. But w h e n the F1 a n d (2) to collect basic biological and genetic data to backcross females were crossed with H. subflexa establish the basis for the sterility. males, normal chromosome pairing, eupyrene Several facts have emerged from this research. transfer, a n d fertility w e r e restored in the b a c k c r o s s Hybrids were produced from both interspecific males (Proshold, unpublished data). In another c r o s s e s (Proshold a n d L a C h a n c e 1974). In the study, it was possible to transfer a dominant mutant laboratory, behavior a n d mating p e r f o r m a n c e of g e n e f r o m H. virescens to H. subflexa by crossing the two types of hybrid males were similar. Sterility H. subflexa females with mutant H. virescens was characterized by a lack of eupyrene sperm in males a n d crossing mutant hybrid a n d b a c k c r o s s the spermatheca, though apyrene sperm were females with H. subflexa males (Proshold, Kar• commonly present. Eupyrene sperm bundles were penko a n d Raulston, unpublished data). produced by hybrid males in fairly normal quanti• Thus, at least two separate types of sterility are ties and were transferred to spermatophores dur• a s s o c i a t e d with Heliothis hybrids. One is asso• ing mating. However, the bundles failed to break ciated with c h r o m o s o m e desynapsis a n d the sub• d o w n within the s p e r m a t o p h o r e a n d the e u p y r e n e sequent spermiogenic abnormalities. This sterility s p e r m w e r e not i n c l u d e d with the material ejected is lost w h e n f e m a l e s are c r o s s e d with the a p p r o p • into the seminal duct (Proshold et al. 1975). Meiotic riate male so that the species g e n o m e is p l a c e d chromosomes from primary spermatocytes exhi- into the s a m e c y t o p l a s m . M o r e importantly f r o m a bited a high d e g r e e of desynapsis (Proshold a n d control standpoint, there is a persistent backcross LaChance 1974) and many of the subsequent male sterility that exists when the H. virescens s p e r m cells c o n t a i n e d a double a m o u n t of D N A in genome is present in H. subflexa cytoplasm. This t h e h e a d , w e r e t w o - or multiple-tailed, a n d p o s • cytoplasmic sterility is maternally inherited. In sessed other duplication deficiency abnormalities some insects, such sterility is associated with mat• (Richard et al. 1975; Goodpasture et al. 1980). ernally transmitted cytoplasmic microorganisms. W h e n hybrid a n d b a c k c r o s s females w e r e This d o e s not s e e m to be the c a s e in Heliothis, at c r o s s e d with either H.subflexa or H. virescens for least for bacterial or rickettsial organisms (La- several generations, chromosome pairing and C h a n c e a n d Karpenko 1981). M o r e probably this sperm duplication deficiency abnormalities in sterility is associated with mitochondrial DNA. The males gradually approached normal (Proshold, mitochondrial D N A of H. virescens is different from u n p u b l i s h e d d a t a a n d G o o d p a s t u r e et al. 1980). If that of H. subflexa, a n d the mitochondrial D N A of H. virescens w a s t h e female in t h e interspecific BC insects is similar to that of H. subflexa ( M . cross, in addition to normal c h r o m o s o m e pairing in Huettel, personal communication). the backcross male, his ability to transfer eupyrene In contrast to hybrid males, hybrid f e m a l e s differ

3 3 0 greatly in appearance, biology, and reproduction with H. virescens males. Further, Pair et al. found depending upon the type of interspecific cross. synchrony in mating time between BC and H. vires• W h e n H. subflexa was the female in the interspe• cens females; however, H. subflexa females mated cific cross, about 40% of the hybrid females earlier in the scotophase than the other two entered an intense diapause from which few females. For the first mating, BC and H. virescens emerged (Laster 1972; Proshold and LaChance females were found in copula with both types of 1974). Most females that did not diapause con• males in about equal proportions, but rematings tained few or no mature eggs and would not mate occurred more frequently with BC males than H. with males of either species. Those that did mate virescens males for both types of females. oviposited only about one-half and one-fourth the Females mated with BC males readily remate. number of eggs oviposited by H. subflexa a n d H. Pair et al. (1977b) found that if the next mating w a s virescens females, respectively. If mated, egg hat- with a H. virescens male, then the female became chability was as great as expected of females of fully fertile. In contrast, if females mated with H. either species (Proshold and LaChance 1974). At virescens males and then with BC males, the least three generations were required before mat• females became infertile to partially fertile. The ing frequency was as prevalent in backcross authors felt this was caused by apyrene sperm of females as that in pure H. virescens (Laster et al. the second mating replacing eupyrene sperm of 1977). the first mating. If these data prove true, then the In contrast, hybrid females from the reciprocal value of the released BC male is greatly enhanced. cross (H. virescens female x H. subflexa male) did In an excellent study, Raulston et al. (1979) not enter diapause. Further, they mated readily with released BC insects in a cotton field and observed either male, and if mated laid about the same interaction between released and native insects. number of eggs as H. subflexa females. However, BC females mated readily with native males, but eggs from these females did not hatch as fre• native females were rarely observed in copula with quently as eggs from either H. virescens or H. BC males. BC males were competitive with native subflexa females (Proshold and LaChance 1974). males for BC females, but not for native females. In When hybrid and backcross females are general, the BC insects' behavior was similar to crossed with H. virescens males, about half of the that of the laboratory colony from which they were remaining H. subflexa c h r o m o s o m a l D N A is derived. Carpenter et al. (1979) observed similar replaced by H. virescens DNA each generation. results with BC females. Thus, the behavior of the Thus, chromosomal DNA of BC3 insects should be BC insects in nature seemed to be dependent upon nearly 9 4 % H. virescens. The persistence of the the genetic background from which the BC origi• backcross male sterility allows the use of insects nated. As Raulston et al. (1979) suggest, this allows that have been backcrossed to the point of being the engineering of behavior in released insects. genetically similar to H. virescens. Thus, most of In a limited cage study in which H. virescens a n d the research comparing the behavior and competi• BC insects were released in ratios of 1:1 or 1:5, tive ability of backcross insects with that of H. vires• Laster et al. (1978b) collected first- and second-

cens was done with BC3 or later generation insects. generation eggs and larvae. Hatchability of first- Sex traps baited with BC females (one/trap) generation eggs was lower in cages with both types caught as many native H. virescens males as ones of insects than in cages with only H. virescens. baited with H. virescens females (Laster et al. When adult males from eggs or larvae from various 1978a). Interestingly, females previously mated to cages were crossed with females, from 59 to 100% BC males seemed to catch more males than virgin of the females failed to reproduce, indicating infu• females caught, which would indicate that BC sion of the male sterility. Infusion of sterility w a s males did not satisfy the mating urge of females also observed following a one-time release in a and they would readily remate. The fact that more semi-isolated plot of cotton and sesame (Martin et males were trapped in the first instance can best be al. 1981 b). Furthermore, emergence from diapause explained by selection. Not all virgin females of BC insects appeared to be in synchrony with that placed in traps have the propensity to mate. Proba• of H. virescens (Martin et al. 1981a; Stadelbacher bly, these females would be precluded in traps and Martin 1981). baited with females mated to BC males. Pair et al. Based on this research, it was believed that a (1977a) found that females mated with BC males concentrated study was warranted on the feasibil• remated about twice as frequently as those mated ity of managing a native population of H. virescens

331 releasing b a c k c r o s s insects. T h u s , in 1977, the tains the highest terrain (highest peak is 3 5 5 m). Agricultural R e s e a r c h Service of t h e U.S. Depart• Rainfall becomes more abundant westward, with m e n t of Agriculture, in cooperation with the Missis• the greatest a m o u n t (about 1270 m m / y e a r ) in the sippi Agricultural and Forestry Experiment Station northwest hills. T h e southwestern portion of St. a n d with t h e College of the Virgin Islands Experi• Croix is much flatter than other parts of the island m e n t Station, b e g a n a 4 - y e a r pilot test program on and was used extensively for sugarcane produc• the island of St. Croix. BC insects w e r e to be reared tion until 1965. Temperatures vary little, either daily in Stoneville, Mississippi, a n d mailed to St. Croix, or seasonally; monthly means range from 22.2 to w h e r e they w e r e t o b e r e l e a s e d . Studies w o u l d b e 29.4°C. Relative humidity averages 55 to 7 0 % a n d c o n d u c t e d on behavior a n d interaction in c o m p a r i • evaporative rates average over 1.8 m per year s o n with native insects, on infusion of male sterility b e c a u s e of t h e easterly trade winds. A short rainy into t h e native population, a n d on the potential for period usually occurs from April through June and s u p p re s s i n g t h e native population by an all-island a longer season from September to December, but release. rainfall is quite variable, with periods of extreme drought o c c u r r i n g frequently. Beginning in N o v e m b e r 1977, a n d prior to the Pilot Test for Release of first release of b a c k c r o s s insects, 42 c o n e traps Backcross Insects w e r e established throughout St. Croix (Figure 1). T h e traps w e r e baited with three virgin females a n d c h a n g e d at least three times weekly. In D e c e m b e r St. Croix—the Site 1978, all traps w e r e modified by inserting a 10.2 cm skirt (Hartstack et al. 1979). St. Croix is o n e of t h e m o r e isolated of the small In addition, up to 11 plots from various locations C a r i b b e a n islands ( M i s k i m e n a n d B o n d 1972). T h e (Figure 1) w e r e selected for study sites. At e a c h site nearest islands are 64.5 km northward. T h e prevail• the t w o most important hosts for t o b a c c o b u d w o r m ing eastwardly winds do not favor immigration from on St. Croix, pigeonpea (Cajanus cajan [L] Millsp.), this direction. W i n d w a r d , the nearest islands are a n d Bastardia viscosa (Koth.) (Snow et at. 1974) 161.3 km away. St. Croix is about 37 km long east to w e r e planted. T w o types of pigeonpea w e r e util• west, a n d 9.7 km w i d e at the widest point, c o m p r i s • ized, o n e (cv N o r m a n ) w a s indeterminate a n d the ing an area of a b o u t 217.6 km2 . T h e eastern o n e - other was a local cultivar that bloomed only during third of St. Croix consists of hills up to 1 5 2 or 183 m the short photoperiod of O c t o b e r to M a r c h . Cv Nor- in altitude. Rainfall here a v e r a g e s b e l o w 5 1 0 mm m a n w o u l d flower about 3 months after planting, annually. T h e northwestern portion of St. Croix c o n - regardless of time of year. Bastardia was an availa-

STUDY SITE CONE TRAP STATION

Figure 1. Cone traps were baited with virgin female backcross insects to monitor male H. virescens and backcross populations. The 11 study sites were planted in pigeonpea and Bastardia to monitor egg and larval populations. St. Croix, U.S. Virgin Islands.

3 3 2 ble host year round, though the suitability varied lecting eggs from these ovipositing females, a n d d e p e n d i n g u p o n rainfall. observing egg hatch; fertile eggs w o u l d have signi• fied introduction of o n e or m o r e H. virescens females into the BC colony. Rearing and Shipping the Insects For colony maintenance and egg production, p u p a e were held until e m e r g e n c e in 3.8-liter c y l i n • O v e r 10 million BC a n d H. virescens pupae were drical cardboard containers. The emerged moths reared by the Bioenvironmental Insect Control were paired a n d held in these containers, w h e r e Laboratory, ARS, U.S. Department of Agriculture, they oviposited on fine-weave polyester cloth (Hill Stoneville, Mississippi, for c o n d u c t of this pilot test and Co., Inc., P.O. Box 15159, Cincinnati, Ohio) during 1 9 7 7 - 1 9 8 0 . During the period mid-August to covering the top of the container and also on a strip m i d - D e c e m b e r 1980, over 5 million BC p u p a e were (about 7.5 cm wide) suspended from the container 2 shipped to St. Croix for release of about 40 t h o u • top edge to the bottom. A 7.5 c m cotton pad satu• s a n d m o t h s / d a y . rated with 5% sucrose solution placed on the cloth Backcross and H. virescens insects w e r e reared cover served as a food a n d water source. Collec• with m e t h o d s a n d diet similar to those reported by tion of moth scales w a s a c c o m p l i s h e d by a d e v i c e Raulston a n d Lingren (1972) for H. virescens, but similar to that described by Hartley et al. (1977). more specifically by Hartley et al. 1982. Larval rear• Eggs produced in these colonies were transferred ing was in a multicellular unit constructed from poly• to a facility described by King et al. (1979) for mass s t y r e n e l i g h t - d i f f u s i o n l o u v e r s fitted into a production of the BC. fiberglass tray filled with insect diet. T h e tray w a s Pupae were p a c k a g e d a n d s h i p p e d using t e c h • covered with porous polypropylene (125-micron niques similar to those reported by Raulston et al. openings) (Porex® , Glassrock, Plastics Group, (1976b). T w o hundred pupae, based on weight, Fairburn, Georgia 30213) followed by reinforce• were placed in 0.47-liter cylindrical cardboard con• ment structure a n d strapping together at e a c h end. tainers filled with dry vermiculite. T h e top of e a c h A diet of s o y b e a n flour a n d wheat g e r m , with c o r n - container was perforated for ventilation and taped c o b grits as a substitute for part of the agar, was shut with 2.5 cm masking tape to prevent spillage of used for larval rearing. Calco red® , an oil-soluble contents. T h e containers were shipped in c o r r u • dye, was a d d e d to the larval diet to mark released gated cardboard boxes (24/box) with ventilation moths and their eggs. holes. Shredded paper was placed around the c o n • tainer in the box to further cushion the pupae during T h e trays containing eggs were incubated a n d shipment. T h e boxes were shipped airmail through larvae reared at 29.5°C a n d 5 0 % RH for 18 days , the U.S. Postal Service. Moth e m e r g e n c e from w h e n the p u p a e were harvested, by first passing pupae p a c k a g e d a n d shipped by this process aver• t h e m through a series of gratings to r e m o v e large a g e d 85%. particles, and then removing lighter particles with an air current from a high-volume blower (Dayton M o d e l 2 C 8 9 0 ) . T h e p u p a e were w e i g h e d to deter• mine the number harvested. E m e r g e n c e of moths Release from these p u p a e a v e r a g e d 8 8 % . Production of the BC required m a i n t e n a n c e of a Four releases were made (Table 1) (Proshold, Heliothis virescens colony to obtain males for mat• unpublished data). T h e first two releases w e r e ing with BC females. T h e s e colonies were m a i n • point releases a n d all insects were released at o n e tained in separate facilities as described by Brewer site on the Federal Experiment Station. T h e third et al. (1978). After the initial sexing with the aid of a release (west release) was m a d e at 10 sites in the s t e r e o s c o p e (Butt a n d C a n t u 1962), male H. vires• western part of St. Croix and the fourth release cens p u p a e were c o n f i r m e d o n c e more before (all-island release) was m a d e at 50 sites t h r o u g h • transfer into the BC colony a n d a s e c o n d time out St. Croix (Figure 2). T h e first release w a s m a d e before setting up for m o t h e m e r g e n c e . BC p u p a e with pupae, the s e c o n d a n d third releases with both were s e x e d only o n c e , to r e m o v e the sterile males pupae a n d adults, a n d the fourth with p u p a e only. to prevent interference in mating b e t w e e n BC T h e first t w o releases were m a d e during the time of females and H. virescens males. M a i n t e n a n c e of year when native populations were the greatest. sterility within the BC c o l o n y w a s monitored twice T h e third release w a s m a d e into an increasing weekly by mating male a n d f e m a l e BC moths, c o l • population following the onset of the rainy period,

3 3 3 and the all-island release was made during the dry were trapped within 0.8 km of the release site and season when the native population was the lowest. another 24% were trapped from 0.8 to 1.6 km from the release site. No male was recaptured further than 16.1 km. Consequently, for the point release Behavior and Interaction of the ratio of R:N males dropped rapidly away from Released (R) with Native (N) the release point, so that ratios of 1 or higher R:N were obtained only within the first 1.6 km. For the Insects third release, ratios of 1:1 or higher were trapped throughout the western part of St. Croix and ratios Released males did not appear to disperse far from of 1 R:2N were trapped in the central area. During release point. Nearly 60% of the males recaptured the final release no trap was further than 1.6 km

Table 1. Dates and approximate number of backcross tobacco budworm (Heliothis virescens) sterile hybrids released on St.Croix, U.S. Virgin Islands, 1979-1960.a

Release area N o . s i t e s D a t e T y p e N u m b e r 1979

S t a t i o n 1 19 Jan-16 Feb Pupal 3 500 females/day 3 500 m a l e s / d a y

S t a t i o n 1 13 Apr-27 Apr Pupal 3 500 females/day 3 500 m a l e s / d a y A d u l t 5 000 m a l e s / d a y

W e s t 10 1 Nov-15 Nov Pupal a n d a d u l t 3 500 females/day 15 Nov-22 Nov A d u l t 3 500 m a l e s / d a y 22 Nov- 19 Dec P u p a l 20 0 0 0 females/day

1980 A l l - I s l a n d 50 27 Aug- 17 Dec Pupal 20 0 0 0 m a l e s / d a y a . The first two releases were conducted for study of behavior and interaction between released and native insects; the third release was made to study infusion of the sterility trait into the native H . virescens population; and the fourth release was made to dem • onstrate suppression of the native H . virescens population by infusion of sterility.

RELEASE CAGES 3rd release RELEASE CAGES 4th release STATION

Figure 2. Sites for the third and fourth releases of the backcross tobacco budworm (Heliothis v i r e s c e n s ; sterile hybrid on St. Croix, U.S. Virgin Islands.

3 3 4 f r o m o n e of the 50 release sites. Within 61 m of greater during all releases. Of a single collection of release sites, R:N ratios were 1 0 : 1 ; from 0.4 to 0.8 native females that were mated, during the point, km, 9 : 1 ; from 0.8 to 1.6 k m , 7 : 1 . west, and all-island release, 92, 81, and 25%, Activity of the insect was studied by the method respectively, were fertile (contained eupyrene of Raulston et al.(1976a) and Lingren et al. (1978). sperm in their spermathecae). This substantiates In general, released insects become active earlier the high degree of mating interactions b e t w e e n than native ones. Of the 395 females collected native females and backcross males. flying, feeding, or ovipositing, three-fourths were released females. For wild females, the ratio of females flying to feeding to ovipositing was the Infusion of Sterility into same before 2000 AST (Atlantic Standard Time) as Native Populations that after 2000 AST. About half were collected fly• ing a n d one-fourth either ovipositing or feeding. Since backcross insects are genetically very sim• Conversely, for released females, 86% were col• ilar to H. virescens, there is no difference in external lected before 2000 AST, a n d of these, over half appearance of the two types. Thus ratios of field- were feeding and about equal n u m b e r s flying or reared backcross (BC) insects to pure H. vires• ovipositing. After 2000 AST, about the same cens (V) were determined by crossing males to numbers of released females were collected feed• virgin females; males that transferred only apyrene ing, flying, or ovipositing. Comparing the numbers sperm were considered BC males (Proshold and of females ovipositing, there was no difference in LaChance 1974). All males trapped alive were ratio of wild and released females, regardless of the crossed. Before any backcross insect was collection time. Ratios of females collected ovipos• released on St. Croix, 400 males collected in c o n e iting on pigeonpea a n d on Bastardia were the traps from October to December 1978 were same. crossed in the laboratory with virgin females to About the s a m e ratio of R:N males were c o l • check the reliability of this method of determining lected either feeding or flying, but before 2000 AST BC males. Of these, 6 6 % mated and of the females a greater percentage were feeding (61%) than that mated, 81% contained sperm in their sper- those collected after 2000 AST (26%). mathecae. Of these, 99.5% contained eupyrene Of females collected in copula, a larger percen• sperm. Only one female received only apyrene tage of released females were collected earlier in sperm. the mating period than were native females. Still, During the release, 268 released males that had s o m e released females were collected in copula as been recaptured in c o n e traps were paired with late as native females. T h e r e was no significant virgin females. Nearly 8 2 % mated a n d of these only difference in time of mating b e t w e e n those females 1 2 % failed to transfer apyrene sperm to the sper- released as adults a n d those put in field c a g e s as matheca. No female contained eupyrene sperm. pupae. Nearly half were collected before midnight. Further, adult males from red eggs (eggs laid by In contrast to ratios of R:N females, released released females) collected on host plants during males, regardless of whether released as adults or the release were also crossed with virgin females. pupae, w e r e collected in copula throughout the For 203 pairs 82% mated, and of those, only 13% night in the s a m e ratios as native males. Slightly failed to transfer sperm. Eight females did contain more than half were picked up before midnight. eupyrene sperm. However, this was probably the Of 1141 pairs picked up in copula, 8 4 % were result of our mistaking embryonated eggs laid by b e t w e e n released females and released males a n d native females for red eggs rather than of the BC 11 % were b e t w e e n released females a n d native males recovering the capacity to transfer eupyrene males. W h e n p u p a e were p l a c e d in c a g e s a n d sperm in BC males. allowed to emerge, mating b e t w e e n released a n d Crossing virgin females with males captured in native insects was random. But when adults were the c o n e traps provided the most data on BC:V released, a greater than expected frequency of frequency. Of the pairs caged, 70% or more mated, released pairs a n d native pairs were collected. and of those, more than 9 0 % of the females c o n • One of the most important observations made tained sperm. T h e percentage of BC males in the during this study was the reduction in fertility of population increased with e a c h release, but the native females during the release. P e r c e n t a g e mat• percentage of sperm transfer remained fairly con• ing o b s e r v e d in native females w a s nearly 8 0 % or stant (Table 2).

335 Table 2. Percent mating, sperm transfer, and percent field-reared backcross tobacco budworm (Heliothis virescens sterile hybrids aa determined by crossing virgin H. virescens females with males trapped on St Croix, U.S. Virgin Islands, following the release of backcross Insects.

I f m a t e d N o . o f M a t i n g female w/sperm B a c k c r o s s Release no. Trapping period p a i r s (%) l%) l%)

1 15 Jan 1979 - 30 May 1979 5 0 7 5 6 9 . 8 9 2 . 4 4.6 2 30 May 1979 - 15 Dec 1979 2 6 1 0 7 1 . 1 9 4 . 1 5.5 3 15 Dec 1979 - 2 Oct 1980 7 8 1 0 7 7 . 1 9 1 . 0 3 3 . 9 4 2 Oct 1980 - 1 Mar 1981 3139 7 5 . 6 9 2 . 8 8 3 . 8

The first field-reared BC male was collected 6 The all-island release began 27 Aug 1980. From weeks after the first pupae were placed in field 17 Sept 1980 to 25 Feb 1981, the rate of increase in cages. During the first field generation, nearly 10% BC frequency per week followed the quadratic of all males that were collected were BC, and at one curve Y = 11.77 + 12.48x - 0.7598x2 + 0.0164 x3, location nearly one-third of the males from one where Y = expected BC frequency and x = week sample period was BC. The location was within 1.6 (Figure 3). Indeed, until the first of D e c e m b e r , the km of the release site. Within the first 3 months, the BC frequency was greater near the release site t h a n at distances of m o r e than 4.8 k m . In fact, no 100 BC male was trapped on the east end until 2 months after the release. Considering all males trapped, the BC frequency declined at a rate of about 2% per month until June. The June popula• tion showed a significant increase in BC percen• 80 tage over the May population (G=32.477, P< 0.001) but there was no difference because of distance (G=3.51,6, D.F.=4, P > 0.75) nor was there any interaction (log likelihood ratio test, Sokal an d Y = 4 1 . 8 7 + 2 . 5 8 X Rohlf 1969). This increase probably resulted from 60- the second release. Thereafter, the BC frequency Y = 2 6 . 1 6 + 6 . 206 X declined to about 3% in August and remained at -0.145 X2 that level until the west release. Y = 1 1 . 7 7 + 1 2 . 4 8 X 2 The BC frequencies began to increase as a -0.7598 X result of the west release in D e c e m b e r . T h e r e w a s + 0.0164 X3 no significant difference between frequencies 40 obtained at release sites and those in the west region. For January, February, and March, these frequencies were about 50%. Fewer BC males were trapped in the central and eastern regions. About three generations were required (December 20 1979 to April 1980) for the BC frequencies to become homogeneous throughout the western S e p t . O c t N o v D e c J a n F e b and central regions. Another generation (until 17 8 0 8 1 2 5 June) was required for complete island-wide homogeneity, at which time the BC frequency was Figure 3. The rate of increase in backcross 23%. This frequency dropped to a low of 18% in tobacco budworm (Heliothis virescens; sterile July. Interestingly, the BC frequency in August was hybrids within the St. Croix, U.S. Virgin Islands, significantly greater (25%) than that in July H. virescens population followed a quadratic (G=4.336, D.F.= 1, P < 0.05), but there was no differ• curve, and Initially, the Increase was linear with ence among sites nor was there any interaction. an increase of 4 to 5% per week.

3 3 6 increase in BC frequency was linear with an ence between those frequencies and those of increase of 4 to 5% per week. During December, males collected as eggs or larvae. increases in BC frequency leveled off somewhat, From February to July 1981, backcross fre• and from then on to the end of February, increased quency dropped from about 94% to 65%, or at a only at a rate of 2% per week. Nonetheless, for a rate of 1.14% per week. At about 6 5 % , BC fre• 6-week period (17 Jan through 27 Feb 1981) the quency leveled off and has been at that level for frequency of BC males in cone traps was 94.3 + more than 3 months. Comparing the 1981 native 6.24%. A two-way analysis of variance indicated no population on St. Croix and Vieques, a neighboring significant difference among weeks or among sec• island, with that of previous years demonstrates tions for the 6-week period. A frequency of 94% that suppression by the release of the backcross would be a ratio of 17 BC to 1 V insect. insects has been achieved (Table 3). BC frequency obtained from mating tables Whether a mixed population of BC and pure H. (Snow et al. 1974) or from crossing adult males virescens will increase or decrease the following collected as eggs or larvae were similar to those generation depends upon the BC frequency, mat• obtained from traps. For example, for five consecu• ing potential of the fertile males, and the reproduc• tive weeks from 6 Mar 1980 to 1 Apr 1980, 50 tive potential of the females (Makela and Heuttel females were placed on nine mating tables; 4, 3, 1978). The latter, in part, is dependent upon the and 2 in the west, central, and east regions.respec- availability of suitable host plants. On St. Croix the tively. The weekly average over all tables was 43.5 availability of host plants is influenced by rainfall ± 6.2%, with tables in the west, central, and east and varies markedly from year to year. The past 3 averaging 49, 46, and 16% BC, respectively. This years have been increasingly favorable for H. compared with an average of 46% obtained for the virescens, as reflected in the spring trap catches same period with traps. Again, 50 females were on Vieques and the August (dry season) trap placed on four tables four different weeks from 15 catches on St. Croix. Our data indicate that a BC Jan to 27 Feb 1981. The average BC frequency frequency of 17:1 will maintain a static population was 91.5 ± 6.26%. during the population-growth phase. The fact that Similar data were obtained from males from field- the BC frequency was still increasing at the end of collected eggs or larvae. Comparing BC frequen• the release indicates that ratios high enough to cies of males trapped and males collected as eggs cause a population decline during the growth or larvae from October, November, and December phase can be achieved simply by releasing insects 1980 and January 1981 gave no significant differ• for a longer period or in greater numbers. ence because of sampling techniques (G=2.999, Some researchers felt that releasing fertile BC D.F.=1, P< 0.05). For the first few generations after females would cause the first field generation to be the point or west release, BC frequencies of males abnormally large, since H. virescens males c a n collected as eggs or larvae were generally greater mate many times. Our data have shown this not to than those from traps. This was probably due to be true. In fact, the field increase between the sampling error, as most eggs and larvae were col• August and January populations was lower in lected near release sites. Once the BC frequencies 1979-1980 and 1980-1981, following the release of obtained from males collected in traps became BC insects, than in 1978-1979, before BC release. homogeneous island-wide, there was no differ• This probably reflects the benefit of releasing ste-

Table 3. Average number of males per trap per week duri ng various population peaks on St. Croix for 1978-1981 , compared with major spring peak on Vieques. Number I n p a r e n t h e s e s I s t h e f o l d I n c r e a s e f r o m t h e A u g u s t p e a k on 8t Croix.

S t . C r o i x Major spring A u g Jan- Feb Major spring p e a k , Y e a r p e a k p e a k p e a k V i e q u e s

1 9 7 8 - 1 9 7 9 0 . 9 7 . 1 ( 8 ) 1 8 . 8 ( 2 1 ) 1.6 1 9 7 9 - 1 9 8 0 1 . 5 9 . 7 ( 6 ) 2 0 . 1 ( 1 3 ) 5 . 0 1 9 8 0 - 1 9 8 1 5 . 5 9 . 5 ( 2 ) 9 . 0 ( 2 ) 1 9 . 7

3 3 7 rile m a l e s a n d the r e d u c e d reproductive potential MARTIN, D.F. 1977. Equipment for mass rearing of the of females mating with t h e s e males. This r e d u c e d g r e a t e r w a x m o t h a n d t h e parasite Lixophaga diatraeae. potential may result through replacement of eupy- U.S. Agricultural Research Service (Report) ARS-S-164 , rene s p e r m f r o m a previous mating with a p y r e n e Washington DC, USA. 4 pp.

sperm (Pair et al. 1977b), or by preventing the HARTLEY, G.G., KING, E.G., BREWER, F.D., and f e m a l e f r o m being fertilized within t h e first few GANTT, C.W. 1982. R e a r i n g of t h e Heliothis sterile nights of emergence, a requirement for maximum hybrid emphasizing a multicellular larval rearing con• egg production (Proshold et al. 1982). tainer and pupal harvesting. Journal of Economic Ento • This unique s y s t e m of using inherited male steril• m o l o g y (in press). ity would seem to have several advantages over HARTSTACK, A.W., WITZ, J.A., and BURK, D.R. other sterility-inducing systems such as radiation 1 9 7 9 . M o t h t r a p s for t h e t o b a c c o b u d w o r m . J o u r n a l o f or chemosterilization: (1) no treatment is necessary Economic Entomology 72: 519-522. other than the original cross; (2) any life stage of the KARPENKO, C.P., and PROSHOLD, F.I. 1977. Fertility insect can be released; and (3) the desired BC a n d m a t i n g p e r f o r m a n c e o f interspecific c r o s s e s f r e q u e n c y c a n be obtained either by release of b e t w e e n Heliothis virescens a n d H. subllexa b a c k - large n u m b e r s for one generation or fewer c r o s s e d for t h r e e g e n e r a t i o n s to H. subllexa. A n n a l s of t h e numbers for several generations. Whether such a Entomological Society of America 70: 737-740.

s y s t e m c a n be f o u n d with other Lepidoptera KING, E.G., HARTLEY, G.G., MARTIN, D.F., SMITH, remains to be determined. But the potential for J.W., and SUMMERS, T.E. 1979. P r o d u c t i o n o f the population suppression by this t e c h n i q u e w o u l d t a c h i n i d Lixophaga diatraeae on its natural host, the make the effort worthwhile. s u g a r c a n e borer, a n d o n a n u n n a t u r a l host, t h e greater wax moth. U.S. Department of Agriculture, Advances in Agricultural Technology 3, Washington DC, USA. Note; T r a d e n a m e s are u s e d in this paper solely for the p u r p o s e of providing specific information. KNIPLING, E.F. 1960. U s e o f i n s e c t s for their o w n d e s • Mention of a trade n a m e does not constitute a truction. Journal of Economic Entomology 53: 415-420 .

g u a r a n t e e or warranty of the product by the U.S. KNIPLING, E.F., and KLASSEN, W. 1976. Relative effi• Department of Agriculture or an endorsement by c i e n c y of v a r i o u s g e n e t i c m e c h a n i s m s for s u p p r e s s i o n of the Department over other products not mentioned. insect populations. U.S. Department of Agriculture T e c h • nical Bulletin 1533, Washington DC, USA. 56 pp.

LaCHANCE, L.E., and KARPENKO, C.P. 1981. Effect of s e v e n antibiotics on t h e g r o w t h a n d r e p r o d u c t i o n of References Heliothis subllexa x H. virescens interspecific h y b r i d s a n d backcross males. Annals of the Entomological Society of A m e r i c a 74: 4 9 3 - 4 9 7 . BREWER, F.D., GANTT, C.W., and MARTIN, D.F. 1 9 7 8 . M e d i a p r e p a r a t i o n a n d b r o o d c o l o n y facility P a g e s LASTER, M.L. 1972. Interspecific hybridization of Helio• 7 2 - 7 5 in Facilities for insect research and production, this virescens a n d H. subllexa. Environmental Entomol• eds. N.C. Leppla and T.R. Ashley U.S. Department of o g y 1 : 6 8 2 - 6 8 7 . Agriculture technical bulletin 1576, Washington, DC, LASTER, M.L., MARTIN, D.F., and PARVIN, D.W., Jr. USA. 1 9 7 6 . Potential for suppressing tobacco budworm (Lepi• BUTT, B.A., and CANTU, E. 1962. S e x d e t e r m i n a t i o n o f doptera: Noctuidae) by genetic sterilization. Mississ i p p i lepidopterous pupae. U.S. Department of Agriculture, Agricultural and Forestry Experiment Station technical ARS-33-75, Washington DC, USA. 7 pp. bulletin 82, Jackson, Miss.. USA. 9 pp.

CARPENTER, J.E., SPARKS, A.N., and RAULSTON, LASTER, M.L., MARTIN, D.F., and PAIR, S.D. J . R . 1 9 7 9 . C o m p e t i t i v e n e s s of Heliothis h y b r i d s vs. H. 1977. M a t i n g i n c i d e n c e of m a l e Heliothis virescens, virescens f e m a l e s for H. virescens m a l e s in G e o r g i a h y b r i d a n d b a c k c r o s s m a l e s f r o m H. subllexa x H. vires• tobacco. Journal of the Georgia Entomological Society cens crosses. Annals of the Entomological Society of 14: 6 5 - 6 9 . A m e r i c a 70: 2 9 3 - 2 9 5 .

GOODPASTURE, C., RICHARD, R.D., MARTIN, D.F., LASTER, M.L., MARTIN, D.F., and PAIR, S.D. and LASTER, M. 1980. S p e r m c e l l a b n o r m a l i t i e s i n p r o • 1 9 7 8 a . T h e a t t r a c t i o n of w i l d Heliothis virescens m a l e s to g e n y f r o m i n t e r s p e c i f i c c r o s s e s b e t w e e n Heliothis vires• s e x p h e r o m o n e t r a p s b a i t e d with H. virescens a n d b a c k - cens a n d H. subllexa. A n n a l s of t h e E n t o m o l o g i c a l cross females. Environmental Entomology 7: 19-20. Society of America 73: 529-532. LASTER, M.L., MARTIN, D.F., PAIR, S.D., and FURR, HARTLEY, G.G., GANTT, C.W., KING, E.G., a n d R.E. 1978b. Infusion of h y b r i d Heliothis m a l e sterility into

3 3 8 H. virescens populations in field cages. Environmental RAULSTON, J.R., GRAHAM, H.M., LINGREN, P.D., Entomology 7: 364-366. and SNOW, J.W. 1976a. Mating interaction of native and laboratory-reared tobacco budworms released in the LINGREN, P.D., RAULSTON, J.R., SPARKS, A.N., field. Environmental Entomology 5:195-198. and PROSHOLD, F.I. 1978. Tobacco budworm: noctur• nal behavior of laboratory-reared irradiated adults a n d RAULSTON, J.R., SNOW, J.W., and GRAHAM, H.M. native adults in small diverse cropping systems. U.S. 1976b. Large-scale shipping techniques for tobacco Department of Agriculture ARS-W-1 Series, Washingto n budworm pupae. U.S. Department of Agriculture produ c • D C , U S A . tion research report 166, Washington DC, USA. 6 pp.

MAKELA, M.E., and HUETTEL, M.D. 1978. M o d e l for RAULSTON, J.R., LINGREN, P.D., SPARKS, A.N., genetic control of Heliothis virescens. Theoretical and and MARTIN, D.F. 1979. Mating interaction between Applied Genetics 54: 225-233. native tobacco budworms and released backcross adults. Environmental Entomology 8: 349-353. MARTIN, D.F., PROSHOLD, F.I., and LASTER, M.L. 1981. a. Status of hybrid Heliothis pilot test. Pages 150- RICHARD, R.D., LaCHANCE, L.E., and PROSHOLD, 151 i n Proceedings, Beltwide Cotton Production F.I. 1975. An ultrastructural study of sperm in sterile- Research Conference (1981), 5-6 Jan 1981, New hybrids from crosses of Heliothis virescens a n d H. sub• Orleans, La., USA. flexa. Annals of the Entomological Society of America 68: 3 5 - 3 9 . MARTIN, D.F., LASTER, M.L., and PAIR, S.D. 1981b. Backcross progeny from interspecific hybrids of SNOW, J.W., CANTELO, W.W., BAUMHOVER, A.H., Heliothis subflexa x H. virescens: physiological diapause, GOODENOUGH, J.L., GRAHAM, H.M., and RAUL• winter survival and infusion into natural H. virescens p o p • STON, J.R. 1974. The tobacco budworm on St. Croix, ulations. Environmental Entomology 10: 197-200. U.S. Virgin Islands: Host plants, population survey a n d estimates. Florida Entomologist 57: 297-301. MISKIMEN, G.W., and BOND, R.M. 1972. The insect fauna of St. Croix, United States Virgin Islands. N e w Y o r k SOKAL, R.F., and ROHLF, F.J. 1969. Biometry. San Academy of Science Scientific Survey of Puerto Rico a n d Francisco, USA: W.H. Freeman. the Virgin Islands, XIII. 114 pp. STADELBACHER, E.A., and MARTIN, D.F. 1981. Fall PAIR, S.D., LASTER, M.L., and MARTIN, D.F. diapause and spring emergence of Heliothis virescens, H. 1977a. Hybrid sterility: mating dynamics of backcross subflexa, and backcrosses of their hybrid. Environmental progeny from crosses of Heliothis subtlexa a n d H. vires• Entomology 10: 139-142. cens. Annals of the Entomological Society of America 70: 6 6 5 - 6 6 8 .

PAIR, S.D., LASTER, M.L., and MARTIN, D.F. 1977b. Hybrid sterility of the tobacco budworm: effects of alternate sterile and normal matings on fecundity a n d fertility. Annals of the Entomological Society of A m e r i c a 70: 952-954.

PROSHOLD, F.I., and LaCHANCE, L.E. 1974. A n a l y • sis of sterility from interspecific crosses between Helio• this virescens a n d H. subflexa. Annals of the Entomological Society of America 67: 445-449.

PROSHOLD, F.I., LaCHANCE, L.E., and RICHARD, R . D . 1 9 7 5 . Sperm production and transfer by Heliothis virescens, H. subflexa, and the sterile hybrid males. Annals of the Entomological Society of America 68: 31 - 3 4 .

PROSHOLD, F.I., KARPENKO, C.P., and GRAHAM, C . 1 9 8 2 . Egg production and oviposition in the tobacco budworm: effect of age at mating. Annals of the Ent o m o • logical Society of America (in press).

RAULSTON, J.R., and LINGREN, P.D. 1972. M e t h o d s for large-scale rearing of the tobacco budworm. U.S. Department of Agriculture production research report 145, Washington DC, USA. 10 pp.

3 3 9 Discussion — Session 6

During the d i s c u s s i o n on the use of p h e r o m o n e s , it exploited in m a s s trapping as part of a m a n a g e • was emphasized that although catches in phero- ment program. mone traps may not be directly useful in estimating Dr. Rothschild considered that two or three the size of populations in surrounding areas, they pheromone traps would be sufficient for monitoring may be of use in indicating t h e timing of m o t h Heliothis moths over 1 ha and that a lower density buildup. They are being used in Hartstack's model of traps might be sufficient in larger areas. In Aus• a n d give a w a r n i n g of buildup 3 or 4 d a y s in tralia, p h e r o m o n e septa have r e m a i n e d attractive advance of light traps. for about 14 days, but at ICRISAT Center the septa In a discussion of why pheromone-trap catches have proved to be effective for m o r e than 28 days. do not appear to reflect the size of populations, T h e cost of the Heliothis p h e r o m o n e s in the USA Sparks explained that the males differ in their are from $ 3 t o $ 9 / g . response to the traps a c c o r d i n g to the a b u n d a n c e In discussions of trap designs, it was noted that in of virgin f e m a l e s in the area. T h u s , a - c a t c h of 25 the most efficient traps in the USA, the moths move males in a trap c o u l d represent either a very large upwards into the trap, but in those developed else• population in w h i c h most f e m a l e s are virgin, or a where, moths fall down a funnel into the trap. It was very small population within which most of the not considered that this was likely to indicate a females have been mated. However, it was gener• behavioral pattern difference between H. zea a n d ally agreed that pheromones would be useful when H. armigera, but that there was a n e e d to test the m o r e is k n o w n of the behavior of the m o t h s in range of trap designs at each location. As with light differing circumstances. It was considered unlikely traps, there are many factors, including climatic that t h e Heliothis p h e r o m o n e s c o u l d be usefully ones, that influence catches in pheromone traps.

3 4 0 Session 7

Integration of Management

Chairman: K.S. Kushwaha Rapporteurs: A.B. Mohammed Cochairman: K. Leuschner S.L. Taneja

Past and Future Heliothis Management in Australia

A.G.L. Wilson*

Abstract

H e l i o t h i s punctigera and H. armigera are serious pests of cash crops in Australia, particularly cotton, oilseeds, horticultural crops, and coarse grains. H. punctigera additionally occurs on pasture legumes and weeds. There is increasing evidence of migratory behavior of H. punc• tigera, which tends to move from vegetation of low or zero economic value to crops of high economic value, thus complicating areawide control measures. H.armigera appears somewhat more sedentary, but also shows the same crop-succession tendencies. Heliothis management still relies predominantly on use of insecticides. With cotton, where cost of control is heaviest, economic and biological injury thresholds have been devel• oped and are used in conjunction with regular crop scouting to minimize spray frequency. The various processes have been integrated in a computerized decision-making program, SIRATAC, to optimize spray timing. The same sequence of developments may be applied to other crops in future. Some progress has been made towards a biologically orientated pest-management ap• proach, including use of resistant varieties, parasites, predators, pathogens, and selective insecticides. Used singly, none of these components is very effective, and in no crop have enough components been assembled to give a commercially viable management program particularly because sudden upsurges of H e l i o t h i s can only be combated successfully with ''hard'' insecticides. However, some of the biological control components are compatible with insecticidal control and are being incorporated into management systems based on it.

*Commonwealth Scientific and Industrial Research Organization, Division of Plant Industry, Cotton Research Unit, Narrabri, NSW, Australia.

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1961, Patancheru, A.P., India 3 4 3 To give a background for subsequent discussion of flower are the most important crops infested. Cot• Heliothis management a summary is first pres• ton accounted for 46% of the estimated total cost of ented of the host range, economic status, biology, Heliothis control in Australia of $23.5 million. In and control of Heliothis spp in Australia. addition to the costs of control, damage caused to unprotected crops and residual damage where protection is incomplete may approximately double Species and Their Distribution the cost of Heliothis infestation. Besides the crops listed, fodder lucerne (alfalfa) and fruit trees ma y T w o Heliothis species are of economic importance also be infested by H. punctigera in outbreak years in Australia: Heliothis punctigera Wallengren, the at levels requiring control measures, while spraying native budworm, and H. armigera (Hubner), the may also be carried out on intensive horticultural cotton bollworm, or corn earworm. H. assulta crops, the area of which is small. G u e n e e a n d H. rubrescens (Walker) also occur, Secondary pest outbreaks may occur as a result but have not so far been recognized as pests of control measures for Heliothis. Thus severe (Common 1953). H. punctigera occurs only in Aus• tralia, where it is recorded in all states. H. armigera, 3 an economic pest in many countries, is usually less H. punctigera abundant. It is not reported from Tasmania or South H. armigera Australia and is of only minor importance in 2 Victoria. O r d ( 1 5 ° S ) Mean 1970-1974 The period of activity and relative abundance of 1 the two species are illustrated by graphs of light- trap catches at three locations (Fig. 1). H. punctig• era alone is active between September and April 0 (i.e. spring to autumn) near Adelaide, South Austra• 6 lia. Both species are represented at Narrabri, cen• Narrabri (30°S) tral northern New South Wales, but H. punctigera is Mean 1973-1980 usually the most abundant. Both species are 5 represented all year round in the Ord Irrigation Area, northwestern Australia, but H. armigera was 4 the dominant species after grain sorghum produc• tion commenced in 1969. 3 Pest Status 2 Both species attack a wide range of economically important plants. H. armigera tends to favor grami• 1 naceous crops, while H. punctigera tends to favor broad-leaved crops and weeds. However, both species attack cotton, H. punctigera predominating 0 early and mid-season, while H. armigera may be 3 important towards maturity (Wilson and Greenup Adelaide (35°S) 1977). Mean 1964-1968 (Source: Cullen 1969) The major crops affected by Heliothis s p p are 2 shown in Table 1. To obtain an estimate of eco• nomic losses caused by Heliothis spp in Australia, 1 the Queensland survey of Alcock and Twine (1980) has been expanded by consultation with entomolo• 0 gists in other states. Records of crop area and A S O N D J F M A M J J A production during 1979-80 were obtained from the S p r i n g S u m m e r A u t u m n Australian Bureau of Statistics. W i n t e r In terms of cost of insecticidal control, cotton, Figure 1. Mean monthly catch of H. punctigera tobacco, tomato, sorghum, field peas, and sun- and H. armigera at three sites in Australia.

3 4 4 T a b l e 1 . Statistics o f c r o p s I n f e s t e d b y H e l i o t h i s s p p i n Australia with injury thresholds, insecticide applicati o n * , a n d c o n t r o l c o s t s .

C o s t / h a o f C o s t / h a All-Australia A r e a G r o s s Larval damage A v e r a g e o n e a p p l i c a t i o n (% o f A v e r a g e c o s t o f Heliothis g r o w n V a l u e / h a t h r e s h o l d / n o . o f modal sprayc g r o s s c o s t / h a c o n t r o l a m 2 C r o p species ( 0 0 0 h a ) ( $ A ) P l a n t s p r a y s ( $ A ) v a l u e ) <$ A ) ( $ A m i l l i o n )

T o b a c c o a & p 7 . 5 6 3 4 6 0 . 0 5 0 . 0 3 7 . 5 0 2 3 - 2 0 ( 2 & 3 ) 0 . 4 1 7 4 . 0 0 1 . 3 T o m a t o a & p 8 . 4 4 5 0 7 pb 1 2 . 5 0 1 4 . 3 0 ( 1 ) 0 . 3 1 7 7 . 5 0 1 . 5 C o t t o n a & p 7 5 . 0 1 7 0 0 1 - 4 9 . 5 0 1 5 . 2 0 (1 & 3 ) 0 . 9 1 4 4 . 0 0 1 0 . 8 G r e e n b e a n a & p 7 . 2 1 0 6 8 0 . 3 2 . 2 5 2 3 . 2 0 ( 2 ) 2 . 2 5 2 . 2 0 0 . 4 S w e e t c o r n a 2 . 8 6 7 4 P 6 . 1 0 2 3 . 2 0 ( 2 ) 3 . 4 1 4 1 . 5 0 0 . 4 L u c e r n e s e e d P 1 1 . 0 4 8 5 P 2 . 0 0 1 4 . 3 0 ( 1 ) 2 . 9 2 8 . 6 0 0 . 3 S o y b e a n a & p 5 6 . 0 3 2 0 0 . 5 1 . 2 5 1 4 . 3 0 ( 1 ) 4 . 5 1 7 . 9 0 1 . 0 S o r g h u m a 5 1 8 . 0 2 0 0 1 5 - 3 0 1 . 0 0 . 2 5 2 3 . 2 0 ( 2 ) 1 1 . 6 5 - 8 0 3 . 0 F i e l d p e a P 5 3 . 0 1 9 0 P 2 . 5 0 1 4 . 3 0 ( 1 ) 7 . 5 3 5 - 5 0 1 . 8 1 9 0 L i n s e e d P 1 7 . 0 1 5 - 2 0 0 . 5 0 1 4 . 3 0 ( 1 ) 7 . 5 7 . 2 0 0 . 1 S a f f l o w e r a & p 5 3 . 7 1 4 2 5 1 . 0 0 1 4 . 3 0 ( 1 ) 1 0 . 0 1 4 . 3 0 0 . 8 R a p e s e e d a & p 4 1 . 6 1 4 1 1 5 - 2 0 0 . 5 0 . 2 5 1 4 . 3 0 ( 1 ) 1 0 . 0 3 . 6 0 0 . 1 S u n f l o w e r a & p 2 2 1 . 0 1 3 0 1 5 - 2 0 2 . 0 0 . 5 0 1 4 . 3 0 ( 1 ) 1 1 . 0 7 . 1 0 1 . 6 1 3 0 0 . 4 F i e l d l u p i n e P 1 0 5 . 0 1 5 - 2 0 0 . 5 0 . 2 5 1 4 . 3 0 ( 1 ) 1 1 . 0 3 . 6 0 a. a = H. armigera; p = H. punctigera b . Protective spray c. Modal sprays: (1) endosulfan, 735 g ai/ha; (2) methomyl, 452 g ai/ha; (3) fenvalerate, 90 g ai/ha. tetranychid mite a n d aphid infestations are Host-Plant Succession reported f r o m cotton a n d s e e d l u c e r n e following application of DDT or pyrethroids for Heliothis During t h e w a r m e r months, both s p e c i e s exist on a control. s u c c e s s i o n of hosts. In the N a m o i Valley the s e q u e n c e of major host plants, supporting s u c c e s • sive generations, appeared to be: Pest Biology H. armigera—wheat; preflowering cotton a n d H. punctigera is an opportunist pest, with a high rate s o r g h u m ; f l o w e r i n g c o t t o n , s o r g h u m , a n d of reproduction under favorable conditions and sunflower; strong migratory tendencies. Endemic populations H. punctigera—field lupines, rapeseed, m e d i c s ; are present in the higher rainfall areas of the conti• weeds and preflowering cotton; flowering cotton, nent, but outbreaks occur at irregular intervals sunflower, soybean, a n d lucerne ( W a r d h a u g h et al. (Common 1953). Then heavy spring populations 1980; Wilson unpublished). are t h o u g h t to d e v e l o p on the western plains of N e w South W a l e s a n d Q u e e n s l a n d a n d extend t o In the Namoi Valley, as indicated by the light-trap t h e e a s t e r n s e a b o a r d a n d b e y o n d , c a u s i n g severe catches (Fig.1), populations of H. punctigera infestations of cultivated crops. decline m o r e rapidly in the a u t u m n t h a n those of H. An e x a m p l e of s u c h a migration o c c u r r e d in armigera, which is thus generally more abundant in November 1973, following the outbreak season of autumn. Near Adelaide, H. punctigera infests field 1 9 7 2 - 7 3 . Flights of H. punctigera and other known peas a n d lucerne f r o m early spring to s u m m e r . In migrants Agrotis infusa (Boisduval) and Plusia the O r d Irrigation A r e a s u m m e r , w e t - s e a s o n , infes• (Chrysodeixis) argentifera (Guenee) reached New tations of both species o c c u r r e d on cotton. H. Z e a l a n d , 2 0 0 0 km to the southeast (Fox 1975). A armigera alone infested the d r y - s e a s o n crops of similar e a s t w a r d migration o c c u r r e d in the 1980-81 wheat a n d s o r g h u m , giving rise to heavy m o th season, but infestations were limited by drought in abundance in August-September, when these cultivated areas. crops matured (Fig.1). In contrast, H. armigera a p p e a r s to be a s o m e • w h a t m o r e sedentary pest in Australia, mainly a s s o c i a t e d w t h c r o p hosts, particularly s o r g h u m , Mortality Associated maize, a n d c o t t o n . However, m o v e m e n t of moths with Heliothis spp b e t w e e n c r o p s is thought to o c c u r within regions.

Natural Mortality Overwintering Parasites, predators, pathogens, and physical fac• P u p a e of H. armigera enter a facultative d i a p a u s e tors have been associated with mortality of Helio• d u r i n g t h e winter months, moths e m e r g i n g in this life stages in Australia. The various findings are O c t o b e r - N o v e m b e r (Wilson et al. 1979). s u m m a r i z e d below: T h e proportion of p u p a e entering d i a p a u s e is higher in t h e cooler (southerly) t h a n in w a r m e r Parasites (northerly) parts of the continent. Although both s p e c i e s s h o w a similar r e s p o n s e to temperature in Eggs. Generally, egg parasitism by Trichogram- terminating diapause, moths of H. punctigera matidae a p p e a r s higher in t h e north of the conti- appear about 4 weeks earlier than those of H. nent, with levels of up to 9 0 % b e i n g reported on armigera in t h e spring in s o u t h e r n Australia. s o r g h u m in the O r d Irrigation A r e a ( M i c h a e l 1973). The early emergence permits the former species L o w e r levels are reported in southern Q u e e n s l a n d , to exploit t h e spring flush of growth on pastures a n d w h e r e the Scelionid Telenomius sp is m o r e impor• oilseed crops better than H. armigera. It m a y be tant (Twine 1981). Egg parasitism is virtually non• explained either by s u c c e s s f u l establishment of a e x i s t e n t i n n o r t h e r n N e w S o u t h W a l e s . small nondiapausing segment of the population, Paradoxically, effective parasitism of Heliothis on which emerges from late winter onwards, or by tomatoes by Trichogramma ivelae Pang & C h e n is migration from elsewhere. reported from central Victoria (McLaren 1981).

3 4 6 Larvae. The Braconid Microplitis sp is the most Pathogens important parasite emerging from larvae. It is reported from all states except Victoria and Tasma• Five diseases of the Heliothis larva have been nia. Parasitism levels of 31 % of third- to fifth-instar reported from Queensland (Teakle 1977). The larvae are reported from tobacco (Titmarsh 1981). nuclear polyhedrosis virus disease is the most des• Several Tachinid parasites of larvae have also tructive; outbreaks have been recorded in lucerne, been identified, but their incidence is usually less peanut, sorghum, and unsprayed cotton, where lar• than 5%; of these, Chaetophthalmus sp appeared val infestation levels were high. Outbreaks appear the most widespread. to be most common in moist, cloudy weather. A granulosis virus disease is also reported, but is less Pupae. Of Ichneumonidae and Tachinidae infective. reared from pupae or prepupae, Heteropelma Two fungus diseases, Nomuraea rileyi a n d scaposum (Morley) and Carcelia noctuae C u r r a n Beauveria bassiana also require moist conditions were respectively the most common. An average of to be infective. 18% parasitism of overwintering pupae and prepu• The protozoan disease Nosema heliothidis is pae was recorded in a 6-year study in the Namoi debilitative to Heliothis larvae and may also cause Valley, New South Wales (Wilson unpublished), mortality. while 8 to 18% were found to be parasitized during the summer in sunflower (Forrester and Kay 1981). Both species were found to overwinter within the Physical Mortality host and emerge in the spring. The nematode Heterorhabditis bacteriphora has been identified Heavy physical mortality of eggs and small larvae from Heliothis pupae in south Australia. has been recorded in tobacco and cotton. Only 5 to 10% of eggs laid survived to produce second-instar Predators larvae in studies conducted on tobacco in Queens• land (Titmarsh 1981). Desiccation of eggs and their Room (1979a) obtained evidence that 19 species dislodgment by wind or rain were the major causes of insect and five species of spider could feed on of egg loss, while small larvae disappeared without Heliothis spp in cotton in New South Wales. trace or were found desiccated. In cotton, less than Similar lists of predators have been produced in 10% of eggs counted produced established larvae Queensland. When ranked according to frequency in seedling and early flowering stage of develop• of occurrence, Nabis capsiformis was by far the ment, but the percentage rose to over 50% in later most common in all localities in cotton crops. It is of stages of crop development, when the crop canopy interest that the Anthocorid, Orius sp, did not occur had closed between the rows (Wilson 1981a, in cotton, although common on sunflower, where it 1981b). was the second most common predator after Cam• pylomma livida. In spite of the range ot natural enemies present in Chemical Control unsprayed cotton, yields were 50 to 90% below those in otherwise comparable sprayed cotton in Between the 1950s and the early 1970s, control of New South Wales. Damage was primarily due to Heliothis infestations was largely by DDT. Endosul- the Heliothis spp, but in addition, Earias huegeli, fan or other alternatives were used where conser• Anomis flava, a n d Thrips imaginis contributed to vation of bees was a consideration or where use of losses (Wilson and Greenup 1977). DDT against Heliothis caused upsurges of secon• Natural enemies appear more effective in sun• dary pests such as mites or aphids. flower crops where, particularly with early crops Insecticide resistance was first suspected in H. sown in spring, heavy oviposition at flowering has armigera in the Ord Irrigation Area in 1970 and been noted to produce few larvae. The predatory confirmed in 1972 (Wilson 1974). In laboratory topi• bugs Campylomma livida a n d Orius sp are thought cal application tests, H. armigera showed a 90-fold to be responsible for heavy predation (Forrester resistance to DDT, a five-fold resistance to DDT- 1981). toxaphene and endosulfan, and a three-fold resist• Little information is available on the effects of ance to methyl parathion. No resistance was natural enemies on Heliothis in other crops. detected with DDT and endosulfan in H. punctig-

347 era, although the L D 5 0 values obtained w e r e has, until now, been based largely on chemical somewhat higher than those obtained subse• control. However, there is potential for other ele• quently in N e w South Wales. ments of management (Table 3). Passive manage• Resistance to DDT-toxaphene, which became ment, involving the withholding of sprays when the standard insecticide, increased until in 1974, 50 insect abundance is low, or when natural control s p r a y s w e r e applied in a s e a s o n , at a cost of factors are effective, is recognized as a first step to $175/ha, without adequate control. In the absence reducing insecticide use. There is, however, still a of economically priced alternative insecticides and tendency to apply routine protective sprays against with other increases in production costs, cotton- Heliothis to medium-value crops at a stage of g r o w i n g in the O r d w a s a b a n d o n e d in 1975. development when past experience has shown In the Namoi Valley, over 200-fold resistance of damage can occur. Farmers may alternatively H. armigera to D D T d e v e l o p e d in 1973, a n d 15-fold spray at the first sign of infestation. Such measures resistance was also shown to DDT-toxaphene, are taken partly because of lack of information on c o m p a r e d with a susceptible strain (Table 2) the damaging potential of pest populations, and (Goodyer et al. 1975). However, DDT-toxaphene partly because of difficulty in controlling infesta• c o n t i n u e d to be effective, a n d in spile of its c o n • tions o n c e established in the c r o p c a n o p y . tinued use, the resistance level actually fell to three-fold by 1980, when DDT was withdrawn in favor of newer, environmentally safer, insecticides. Damage Thresholds The fall in resistance level suggests dilution of res• istance genes by moths produced in unsprayed T h e s e considerations indicate the n e e d for crops. The most likely source of such moths was i m p r o v e d information on the d a m a g i n g ability of crops of sorghum and maize, which were not regu• Heliothis in various crops. Such information is a larly s p r a y e d , g r o w n to the north a n d south of the prerequisite to development of integrated pest- heavily sprayed cotton-growing area. The syn• management programs. thetic pyrethroids, methomyl, and endosulfan are A simple approach to determination of economic currently the most commonly used chemicals for injury thresholds involves the calculation of the Heliothis control in Australia. marginal value of sprays in terms of crop loss. Thus, in crops of low gross value per hectare, such as sunflower and other oilseed crops listed in Table Future Management of Heliothis 1, a 1 0 % or 11 % loss may be sustained before the in Australia cost of a spray application equals the value of the yield loss. With the m o r e valuable crops, a loss of less t h a n 1 % c r o p value may justify spraying. As Reduced Pesticide Usage Table 1 shows, this approach is either consciously or unconsciously applied in determining the aver• A c t i v e m a n a g e m e n t of Heliothis spp in Australia age spray f r e q u e n c y in farming practice.

Table 2. Resistance levels of H. armigera to Insecticides (LD5 0 expressed as µg Insecticide per larval weight 35 mg).

Insecticides U n s p r a y e d O r d 1972 Wee Waa 1 9 7 3 Wee Waa 1980

DDT Toxaphene 0 . 7 3 10.6 1 1 . 5 4.5 DDT 0 . 3 5 8 0 . 7 > 1 0 0 . 0 0.9 E n d o s u l f a n 0 . 6 0 3.2 6 . 0 0.6 Fenvalerate 0 . 0 4 0 . 0 4 Methyl Parathion 0 . 0 6 6 0.6 0 . 3 5 0 . 2

Source: 1980 data from New South Wales Department of Agriculture, Resistance Testing Section, Tamworth, Australia.

3 4 8 Table 3. Status of four potentiala pest-management components on various crops In New South Wales (NSW) and Queensland QD, Australia.

H o s t - p l a n t Insecticides r e s i s t a n c e P a t h o g e n s Natural enemies C r o p NSW Q D NSW Q D NSW Q D NSW Q D

C o t t o n H H M M M M L H S o r g h u m M M M M H H M H T o b a c c o H H H H L L M M T o m a t o H H L L L L L L N a v y b e a n . s o y b e a n H H M M H M M S u n f l o w e r M M L L M H H a. H = high potential; M = moderate potential; L = low p o t e n t i a l

Biological Injury Thresholds South W a l e s (Wilson and G r e e n u p 1977). Although compensation as a technique for minimizing spray Only in s o m e of the more valuable crops have application worked successfully in the tropical Ord detailed experiments been d o n e to establish injury Irrigation Area for a f e w years (Wilson et al. 1972), it thresholds under a range of infestation levels a n d b e c a m e impossible to regain control following the stages of c r o p development. A t o b a c c o pest pre• development of resistance, while natural e n e m i e s diction service has bee n d e v e l o p e d in Q u e e n s l a n d . alone did not sufficiently suppress infestations. Unsprayed plots are monitored for eggs and larvae, a n d a d v i c e given to farmers on the timing of sprays if larval survival occurs (Titmarsh 1981). Crop Scouting Both the biological and economic injury thre• sholds of larval a b u n d a n c e in grain s o r g h u m have Improved crop scouting has in itself led to a sub• b e e n d e t e r m i n e d in Q u e e n s l a n d (Twine, these stantial reduction in spray application. Initially car• Proceedings). ried out by farmers or chemical company Heliothis d a m a g e to cotton in Australia may representatives, the task of scouting c o t t o n has o c c u r at any time from cotyledon d e v e l o p m e n t to recently been largely taken over by private consul• boll maturity, a n d it is difficult to assess the effect of tants working on a contract basis. any o n e infestation on final yield. In addition, the This has led to improved, impartial decisions on high c o s t s of production a n d high potential returns w h e n to spray. Although consultants c h a r g e about m a k e this c r o p very sensitive to e c o n o m i c loss. $20/ha per season for this service, this is easily Experiments were carried out in the N a m o i Val- offset by the saving of the cost of o n e or t w o sprays. ley in which protection was omitted or varied in one With better knowledge of the d a m a g i n g potential of of three stages of c r o p development. It w a s f o u n d pests, improved c r o p scouting, a n d more effective that egg survival was lower while the tolerable lar- pesticides, the number of insecticide applications val infestation was higher to flowering. A treatment has fallen f r o m 16 to 20 in 1972-73 to 8 to 11 in the threshold (action level) of four eggs or two small 1980-81 season. larvae/m2 was indicated at that development stage, while the threshold is subsequently r e d u c e d to o n e l a r v a / m2 . Protection is not normally required SIRATAC—Computerized before square production commences or after it Decision-Making Program ceases (Wilson 1981b). B e c a u s e of the relatively short growing s e a s o n To integrate the various factors involved in m i n • and unpredictable climatic conditions, the ability of imizing pesticide applications, a c o m p u t e r i z e d cotton to c o m p e n s a t e for losses c a n n o t be exploit• decision-making "package" has been d e v e l o p e d ed to an a p p r e c i a b l e extent in the main production by CSIRO a n d t h e N e w South W a l e s D epart ment of regions of southern Q u e e n s l a n d a n d northern N e w Agriculture ( P e a c o c k 1980; R o o m a n d H e a r n

3 4 9 1979). The essential components of the system control compatible with a predominantly insectici• are: dal approach.

1. Standardized crop-sampling procedures, in which presence or absence of Heliothis eggs, lar• Resistant Varieties vae, other pests, and natural enemies are observed on 30 plants/40 ha at 3-day intervals and the In the past 20 years, Australian plant breeders have observations marked on cards for computer increased efforts to identify heritable traits for res• processing. istance to Heliothis and other pests and to incorpo• rate these into commercial cultivars. A problem has 2. Weekly counts of squares, flowers, and bolls. been the lower yields or quality often associated with resistant traits, in comparison with commercial 3. Computer processing of the data to estimate cultivars. infestation level/m2 on that day and on the 2 follow• Physiological, morphological, and chemical ing days, taking into account temperature and esti• characters are being incorporated and selected. mated egg and larval survival. For example, in

4. Comparison of crop development with a crop Cotton: earliness; ability to compensate for trajectory, to see whether crop development is losses; glabrous, okra leaf, frego bract, and nectari- behind or ahead of target. less characters; high terpenoid and tannin content (Thomson and Lee 1980). 5. Determination of the dominant species, H. Soybean and navy bean: antibiotic chemical punctigera or H. armigera, by pheromone or light- characters (Rogers 1980). trap catches. Sorghum: increased grain size and ability to 6. Assessment of whether the larval population is compensate for grain losses (Wilson 1975). above the action level for a given phase of crop Of the various traits being investigated in cotton, production. combination of glabrous leaf and frego bract in a Deltapine background is farthest advanced, and 7. Advice to farmer or his consultant (Table 4 and lines have now been released commercially (N.J. 5) on whether a spray is required. Thomson, personal communication).

8. Advice on sprays to be used, on a scale from "soft" (i.e. endosulfan, Bacillus thuringiensis- Pathogenic Microorganisms chlordimeform mixture) to "hard" insecticides (i.e. pyrethroids or organophosphates), taking into Two commercially marketed pathogens have account the species represented. become available in Australia: Bacillus thuringiensis and the nuclear polyhedrosis virus. The SIRATAC service has been well received by B. thuringiensis has been available for 20 years, the cotton-growing community. At present it is but although strains and formulations have operated from terminals connected by telephone to improved over that time, it has not proved suffi• the central computer; however, a simplified pro• ciently effective to be used alone for Heliothis c o n • gram may be developed for cassette operation on trol. However, the mixture with chlordimeform has minicomputers in the field. The program is being been used to a limited extent for several years and extended to give advice on irrigation timing, and has given effective control of Heliothis early in the may later cover other facets of cotton growing. season. An advantage is the delayed buildup of tetranychid mite infestations, which tend to be heavier if broad-spectrum pesticides are used Insecticidal Control Integrated with early in the season (Wilson 1981a). Other Forms of Control The nuclear polyhedrosis virus in the commer• cial formulation Elcar has been assessed experi• A second step towards minimizing insecticide mentally in cotton, sorghum, beans, and maize. application is the development of other forms of Acceptable control of Heliothis larvae has been

3 5 0 Table 4. Specimen farmer output from SIRATAC computer program—crop development.

WONDERCOTT COTTON FARMS INC. REPORT FOR 03-FEB-81

SQUARES & BOLLS COUNTED, CROP DEVELOPMENT AND PROSPE CTS ON 3 FEBRUARY

FRUIT PRODUCTION PLAN (YIELD DEVELOPMENT THRESHOLD)

EFFECTIVE FLOWERS PLANNED ACTUAL/LIKELY TARGET YIELD 5.0 BALES/HA FIRST 1 JANUARY 17 DECEMBER TARGET BOLLS 8 0 . 0 P E R SQ M LAST 7 MARCH 4 MARCH LAST EFFECTIVE FLOWER PLANNED LATER THAN LIKELY

PLANT POPULATION DENSITY 15.0 PER SQ M

NUMBERS OF FRUIT (PER METRE)

LIKELY TO CONTRIBUTE TO HARVEST COUNTED WITHOUT PLANNED DAMAGE (YOT)

SQUARES 6 6 . 7 2 . 9 3 7 . 5 GREEN BOLLS 1 6 9 . 7 9 1 . 0 3 5 . 9 BOLLS BY 7 MARCH 9 4 . 8 9 4 . 4 8 0 . 1

TIMING OF YIELD DEVELOPMENT

SEASON (DAY DEGREES) 13 DAYS EARLY BOLLS EXPECTED TO SURVIVE ARE LIKELY TO REACH TARGET 32 DAYS EARLY

CROP OPENING0 AT LAST COUNT 6 0 ON 16 MARCH 8 0 ON 8 A P R I L

YIELD POTENTIAL (BALES/HA)

WITHOUT WITH DAMAGE DAMAGE FRUIT NOW ON PLANT 5 . 8 6 5 . 8 1 WITH PREDICTED SQUARES 5 . 9 0 5 . 8 7

351 Table 5. Specimen farmer output from SIRATAC computer program—pest data and pest management advice.

PEST STATUS

MEANS FOR WHOLE FIELD; DENSITIES IN NUMBERS PER SQ M ETRE EXCEPT FOR MITES, APHIDS 6 HONEYDEW, WHICH ARE PROPOR TION OF PLANTS OR TERMINALS INFESTED, AND THRIPS, WHICH AR E MEAN NUMBER PER PLANT.

HELIOTHIS DENSITY TODAYS ? A B O V E THRESHOLD THRESHOLD

W H I T E E G G S 9 . 7 1 BROWN E G G S 4 . 4 5 2 0 . 0 VS+S LARVAE 3 . 4 6 2 . 0 YES M + L L A R V E 0 . 0 0 1 . 0 T O T . L A R V A E 3 . 4 6 2 . 0 YES TOMORROWS : VS+S LARVAE 4 . 1 6 M + L L A R V A E 0 . 6 8 1 . 0 TOTAL LARVAE 4 . 8 3 2 . 0 YES NEXT DAYS : VS+S LARVAE 3 . 9 2 M + L L A R V A E 1 . 7 3 1 . 0 YES TOTAL LARVAE 5 . 6 5 2 . 0 YES TOMORROWS : BROWN EGGS 9 . 2 5 2 0 . 0 - NEXT DAYS : BROWN EGGS 5 . 8 3 2 0 . 0

OTHER PESTS DENSITY TODAYS ? A B O V E THRESHOLD THRESHOLD

APHIDS 0 . 0 0 0 . 9 MITES 0 . 0 0 0 . 6 ROUGH BOLLWORM 0 . 0 0 3 . 0 LOOPERS 0 . 0 0 2 0 . 0 GREEN VEGETABLE BUG 0 . 0 0 2 . 0

POOLEDPREDATORS 0 . 0 0

HELIOTHIS AGE BREAKDOWN VS S M L 2 . 0 8 1 . 3 8 0 . 0 0 0 . 0 0

PEST MANAGEMENT OPTIONS

CHOOSE ONE OF THE FOLLOWING LINES AS YOUR PEST MANAG EMENT OPTION ! OPTIONS PRECEDED BY AN "A" ARE PREFERABLE TO THOSE PR ECEDED BY A "B"

TIMING OF THE SPRAY SHOULD BE BASED ON THE NATURE OF THE CHEMICAL AND THE HeliOthiS NUMBERS THROUGH TIME IN THE ABOVE T A B L E

A ENDOSULFAN B DIPEL/CHLORDIMEFORM

IF "B" OPTION CHOSEN SPRAY WITHIN 24 HOURS

3 5 2 obtained under cloudy, humid conditions on vation would destroy a high proportion of overwin• sorghum and beans in Queensland. On cotton, tering pupae. It appears possible that this action although substantial mortality has been obtained in would be effective, but might require legal enforce• a few instances, most results have been disap• ment; the present minor status of the pest does not pointing. Further research to improve the persist• warrant such action. This approach may, however, ence of the material on cotton and other crops is in have been a merit in the tropical Ord Irrigation Area, progress. where H. armigera was a minor pest until irrigated crops, particularly sorghum, bridged the previously inhospitable dry-season period of May to Sep• Integrated Pest Management tember (Fig.1). Then a crop-free period and cultiva• tion of crop residues may have reduced the A w o r k s h o p on the biological control of Heliothis incidence of the pest during the wet season, when spp in Australia was held by the Queensland cotton was grown (Wilson et al. 1972). Department of Primary Industries in 1980 (QDPI During the summer months in New South Wales, 1981). While there was general agreement on the Heliothis spp show a sequence of infestation from desirability of an integrated pest-management extensive crops and pastures where the damage approach involving resistant varieties, native and threshold is either very high or nonexistent, to introduced beneficial insects, and selective insec• intensive crops where the damage threshold is low ticides, including pathogens, it was clear that pro• (Table 1). At present it appears economically gress towards this objective has been slow. Some impracticable to minimize Heliothis in the extensive of the problems that have arisen are: crops, other than possibly by enhancement of bio• logical control agents. 1. No single component of such a pest- management program is normally highly effective on its own, and it has not been possible to assembl e enough components to achieve commercially References acceptable control and yield in any one crop. ALCOCK, B., and TWINE, P.H. 1981. T h e c o s t of Helio• this in Queensland crops. Pages 1 -10 in QDPI 1981. 2. The higher value crops are often extremely sen• sitive to damage or the value of damage may be COMMON, I.F.B. 1953. The Australian species of Heli- exaggerated by "cosmetic" effects, for example othis (Lepidoptera: Noctuidae) and their pest status. Au s • tralian Journal of Zoology: 319-344. minor damage to sweet corn or tomatoes may render these crops unsalable. CULLEN, J.M. 1969. The reproduction and survival of Heliothis punctigera Wallengren in South Australia. Ph.D. 3. The sudden upsurges of Heliothis spp arising thesis, Waite Agricultural Research Institute, University of from migration into crops from elsewhere tend to Adelaide, NSW, Australia. overwhelm the available natural control factors. FORRESTER, N.W. 1981. Biological control agents of Heliothis spp. in sunflowers. Pages 49-53 in QDPI 1981.

FOX, K.J. 1975. Migrant Lepidoptera in New Zealand. Areawide Control New Zealand Entomology 6: 66-69.

GOODYER, G.J., WILSON, A.G.L., ATTIA, F.I., and Field observations suggest that inter- and intra- CLIFT, A.D. 1975. Insecticide resistance in Heliothis seasonal populations of H. armigera are partially armigera (Hubner) (Lepidoptera: Noctuidae) in the Namoi confined to crop hosts within the Namoi Valley. This Valley of New South Wales, Australia. Journal of th e A u s - is supported by the higher level of DDT resistance tralian Entomological Society 14:171 -173. originally detected within cropping areas than out• HEARN, A.N., and ROOM, P.M. 1979. Analysis of crop side. However, the subsequent decline in resist• development for cotton pest management. Protection ance levels suggests that some movement into the Ecology 1: 265-277. area does occur. The possibility that pest carryover from one sea- KAY, I.R. 1981. Host plant resistance. Pages 29-33 in Q D P I 1 9 8 1 . son to the next could be minimized by thorough cultivation of crop residues during the winter has McLAREN, I.W. The use of Trichogramma sp. in toma• been discussed (Wilson unpublished). Such culti- toes. Pages 54-55 in QDPI 1981.

3 5 3 MICHAEL, P.J. 1973. Natural control for insect pests on Wales. Protection Ecology 3: 311 -325. the Ord. West Australian Agricultural Journal 14:20 7 - 2 0 8 . WILSON, A.G.L., and GREENUP, L.R. 1977. T h e r e l a • PEACOCK, W.J. 1980. SIRATAC management system tive injuriousness of insect pests of cotton in the N a m o i for cotton. Agricultural Gazette of New South Wales 9 1 (4): Valley, New South Wales, Australian Journal of Ecol o g y 2 : 7 - 1 0 . 3 1 9 - 3 2 8 .

QDPI (Queensland Department of Primary Industries). WILSON, A.G.L., BASINSKI, J.J., and THOMSON, 1 9 8 1 . Proceedings, Workshop on Biological Control of N.J. 1972a. Pests, crop damage and control practices Heliothis spp. 23-25 Sept 1980, Toowoomba, Queens• with irrigated cotton in a tropical environment. Co t t o n land, Australia. Growers Review 49: 308-340.

ROGERS, D.J. 1981. Varietal resistance to Heliothis WILSON, A.G.L., HUGHES, R.D., and GILBERT. armigera in navy beans (Phaseolus vulgaris). P a g e s 3 6 - 1972b. The response of cotton to pest attack. Bulletin of 42 in QDPI 1981. Entomological Research 61: 405-411.

ROGERS, D.J., TEAKLE, R.E., and BRIES, H.B. WILSON, A.G.L., LEWIS, T., and CUNNINGHAM, 1 9 8 1 . Evaluation of the Heliothis N.P.V. "Elcar" against R.B. 1 9 7 9 . Overwintering and spring emergence of Heli• Heliothis armigera in navy beans (Phaseolus vulgaris). othis armiger (Hubner) (Lepidoptera:Noctuidae) in the Pages 101-105 i n QDPI 1981. Namoi Valley, New South Wales. Bulletin of Entomolo g i • cal Research 69: 97-109. ROOM, P.M. 1979a. A prototype 'on line' system for management of cotton pests in the Namoi Valley, New South Wales. Protection Ecology 1:245-264.

ROOM, P.M. 1979b. Parasites and predators of Helio• this in cotton in the Namoi Valley. Journal of the Aust r a l i a n Entomological Society 18: 223-229.

TEAKLE, R.E. 1977. Diseases of Heliothis caterpillar. Queensland Agriculture Journal 103: 390-391.

THOMSON, N.J., and LEE, J.A. 1980. Insect resist• ance in cotton. A review and prospectus for Australia. Journal of the Australian Institute of Agricultural S c i e n c e 46: 7 5 - 8 6 .

TITMARSH, I.J. 1981. Two seasons' life tables for Heli• othis spp. on vegetative tobacco in far North Queensland . Pages 114-117 in QDPI 1981.

TWINE, P.H. 1981. The potential role of parasites in the biocontrol aspect of pest management of Heliothis. P a g e s 4 3 - 4 6 i n QDPI 1981.

WARDHAUGH, K.G., ROOM, P.M., and GREENUP, L. 1 9 8 0 . The incidence of Heliothis armiger (Hubner) and H. punctiger Wallengren (Lepidoptera.Noctuidae) on cotton and other host plants in the Namoi Valley of New So u t h Wales. Bulletin of Entomological Research 70:113-13 1 .

WILSON, A.G.L. 1974. Resistance of Heliothis armigera to insecticides in the Ord Irrigation Area, North W e s t e r n Australia. Journal of Economic Entomology 67:256-25 8 .

WILSON, A.G.L. 1975. Varietal responses of grain sorghum to infestation by Heliothis armigera. Experimen• tal Agriculture 12: 257-265.

WILSON, A.G.L. 1981a. Field evaluation of formamidine insecticides and Bacillus thuringiensis for selective con• t r o l of Heliothis spp. on cotton. General and Applied Ento• mology 13:105-111.

WILSON, A.G.L. 1981b. Heliothis damage to cotton and concomitant action levels in the Namoi Valley, New S o u t h

3 5 4 Problems and Progress in Heliothis Management in Tanzania, with Special Reference to Cotton

Brigitte T. Nyambo*

Abstract

Heliothis armigera (H'ubner) is a major cotton pest in Tanzania. It also attacks a number of other cultivated crops, and the role of maize in the seasonal buildup of Heliothis, and hence the damage to cotton, has been established. In cotton, control measures include the use of insecticides and early sowing, based on the pest-avoidance principle and the ability of some varieties to compensate for the loss of early fruiting bodies. Despite the difficulties of weather, which have been a major constraint in the effort to introduce and select for insect-resistant characters in recent years, some progress has been made. Both frego bract and high gossypol characters have given promising results.

The American bollworm, Heliothis armigera makes an ideal host for the second generation Hubner, is one of the major cotton pests in Tanza• (Reed 1965). The generations that build up on nia. It also attacks a number of other cultivated maize later move on to cotton at or around flower• crops, including maize, sorghum, millet, legumes, ing time (usually from mid-February). Conse• sunflower, and tomatoes, but its pest status on quently, the severity of H. armigera infestation on these crops has not been fully established. cotton depends a great deal on the Heliothis p o p u • The population buildup of Heliothis on cotton, lation development on early-sown maize. As a and hence the damage caused, varies from season result, in years of low rainfall, during December an d to season, and depends to a great extent on total January, the infestation on cotton in February and rainfall and its distribution. Most of Tanzania's cot• March is often very low, because of the adverse ton is grown around the southern shores of Lake effect of drought on the maize crop. Low and erratic Victoria in an area known as the Western Cotton rainfall in December and January has been a fea• Growing Area (WCGA). In the WCGA, the rainfall ture in the WCGA in recent seasons, and this has pattern is bimodal, with the short rains usually fall• resulted in low levels of Heliothis on cotton. ing between November and early January, and the In 1964, Reed (1965) recorded an average of main rains occurring from March to May. about 0.23 eggs and 0.15 larvae per plant on The first generation of Heliothis armigera builds unsprayed cotton at Ukiriguru during the flowering up on wild host plants, especially Cleome spp, and period. During the same period in the 1979-80 and moves on to the November-sown maize, which 1980-81 seasons, the average egg and larvae count per plant on unsprayed cotton at Ukiriguru

*Ukiriguru Research Institute, Mwanza, Tanzania. was 0.015 and 0.03, respectively. Records from

International Crops Research Institute (or the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India 3 5 5 L u b a g a (an experiment station 1 0 0 km south of the evaluation of D D T . To date, the list of r e c o m • Ukiriguru) indicated an a v e r a g e of 0.003 e g g s a n d m e n d e d insecticides against H. armigera on cotton 0.041 larvae per plant on u n s p r a y e d cotton. consists of D D T 4 0 % ULV or 7 5 % w.p. at 1000 g a i / h a ; endosulfan 2 5 % ULV at 6 2 5 g a i / h a ; D D T 3 5 % plus methidathion 1 5 % ULV ( a c o m m e r c i a l Control Measures mixture) at 8 7 5 + 375 g a i / h a ; D D T 3 5 % plus for Heliothis phenthoate 2 5 % ULV at 8 7 5 + 6 2 5 g a i / h a ; p e r m e - thrin 5% ULV at 125 g a i / h a ; a n d fenvalerate 4% Cultural Practices ULV at 100 g a i / h a .

S i n c e t h e severity of H. armigera attack on early- Progress s o w n c o t t o n in the W C G A is determined largely by the population building up on early-sown maize, it Monitoring and Forecasting w o u l d h a v e been ideal to ban e a r l y - s o w n maize, thus interrupting the generation preceding that Field monitoring or scouting as practiced in Central w h i c h attacks cotton ( R e e d 1965). S u c h a practice Africa has not so far been s u c c e s s f u l in Tanzania, w a s successfully tried by R e e d at Ukiriguru, where where a fixed spraying regime is still followed. T h e early H. armigera attack on e a r l y - s o w n cotton w a s blanket r e c o m m e n d a t i o n advises farmers to apply light, a n d g o o d yields were a c h i e v e d without c h e m • six sprays at 2 - w e e k or 10-day intervals, beginning ical control. at first flower, 10 w e e k s a n d 8 w e e k s after sowing in H o w e v e r , with t h e present c r o p p i n g s y s t e m , in W C G A a n d t h e E C G A (Eastern C o t t o n G r o w i n g w h i c h f o o d c r o p s are given priority, the r e c o m m e n • Area), respectively. dation is impractical. T h e use of maize as a trap T h e g o v e r n m e n t policy of e n c o u r a g i n g c o m m u • c r o p has also b e e n tried, but w a s a b a n d o n e d nal farming on large block farms, plus the rising b e c a u s e it involved s o w i n g maize at a time w h e n costs of insecticides, m a d e it necessary to reas• labor for w e e d i n g cotton w a s in high d e m a n d . sess the fixed spray regime. It was c o n s i d e r e d that Early s o w i n g of cotton is strongly r e c o m m e n d e d . scouting could r e d u c e spraying costs by withhold• C o t t o n in the W C G A should be s o w n b e t w e e n the ing a spray until a given threshold is reached, a n d e n d of N o v e m b e r a n d the e n d of D e c e m b e r . If the the grouping of the farmers would m a k e the intro• s o w i n g dates are strictly observed, first pick should duction a n d supervision of the scouting t e c h n i q u e be ready in M a y / J u n e . T h e s o w i n g date r e c o m • easier. Consequently, scouting trials were initiated m e n d a t i o n was b a s e d on the fact that in years during the 1971 -72 season in the h o p e of introduc• w h e n H. armigera built up early, the e a r l y - s o w n ing a spraying program based on H. armigera e g g cotton may lose its bottom c r o p but w o u l d c o m p e n • a n d / o r larvae thresholds. sate later by producing a c r o p during the main rains After three seasons' evaluation in the W C G A a n d of April a n d May. T h e present varieties grown in ECGA, it was tentatively c o n c l u d e d that cotton Tanzania are particularly suited to s u c h c o m p e n • spraying could be profitable if based on 0.5 or m o r e satory growth, provided soil moisture a n d soil nut• eggs or 0.2 or more larvae per stand. T h e scouting rients are adequate. T h e c r o p w o u l d also be partly trials c o n d u c t e d in W C G A since the 1 9 7 8 - 7 9 s e a • protected f r o m further severe attacks of H. armig• son have not p r o d u c e d clear-cut results, b e c a u s e era by natural e n e m i e s , w h i c h are m o r e abundant the H. armigera infestation has r e m a i n e d consist• after a heavy Heliothis attack (Reed 1965). Under ently low e a c h season, with no clearly defined conditions that allow the Heliothis population to peaks. Consequently, the thresholds used have build up later rather t h a n earlier, the e a r l y - s o w n been unable to trigger a spray. Even in the ECGA, cotton would already have set its main c r o p a n d where the Heliothis pressure is normally higher, it w o u l d therefore e s c a p e serious d a m a g e . has not bee n possible to formulate a r e c o m m e n d a • tion. W h e r e s o m e of the thresholds have triggered spraying, the net e c o n o m i c return has not c o m • Insecticides pared favorably with the net return obtained from the blanket r e c o m m e n d a t i o n . In T a n z a n i a , apart f r o m early sowing, H. armigera Forecasting of H. armigera in order to w a r n the control on cotton a n d s o m e other c r o p s is by c h e m • farmers of a probable heavy attack has not bee n ical m e a n s . Insecticide-testing b e g a n in 1956, with fully evaluated to date, t h o u g h it c o u l d prove useful.

3 5 6 In 1964, for example, it was possible to warn WCGA, it has been difficult to draw any definite extension officers of the likelihood of a severe H. conclusions. Nevertheless, even under the low armigera attack on cotton. This was based on light- Heliothis pressure, frego bract and high gossypol trap catches, as well as on egg and larval counts on plants have both showed reduced numbers of maize in early January. Heliothis larvae (Treen 1979, 1980, 1981) compared with present commercial varieties (Table 3). Work at llonga in 1979-80 (Hackett and Breeding for Plant Resistance Kabissa 1980), under higher levels of Heliothis infestation, also indicated that the frego bract Ukiriguru (UK) cotton varieties have the ability to character was promising. compensate for loss of fruiting bodies caused either by physiological stress or by insect attack. Brown (1962), working at Ukiriguru, showed that Evaluation of New Insecticides the removal of the early flowers from the UK varieties did not necessarily result in lower yield. The evaluation of new insecticides and formula• Instead, flower removal induced greater structural tions in an attempt to identify a cheap, safe (in and frame development, which could lead to yield terms of mammalian toxicity), and efficient chemi• recovery, provided soil moisture and nutrients were cal to control H. armigera on cotton has b e e n sufficient. emphasized in our research program. In recent work initiated in the 1972-73 season at Wettable powders and emulsifiable concen• Ukiriguru, the possibility of incorporating Heliothis- trates are used in the ECGA by small holders. ULV resistant characters into the UK varieties has been formulations have wholly replaced these in the studied, with emphasis on frego bract, nectariless, WCGA and on large Tanzania Cotton Authority high gossypol, and glabrous characters. The frego (TCA) production farms in the country. Spraying is bract selections gave promising results in the done solely by hand-held sprayers. 1973-74 and 1974-75 seasons (Tables 1 and 2). In addition to the organophosphates, organo- The study was resumed in 1978-79 at Ukiriguru chlorines, and carbamates, the synthetic and initiated at llonga in the ECGA during 1979-80. pyrethroids have also been examined, and some of However, due to the low pest pressure in the them have been recommended for farmers' use.

Table 1. Bollworm damagea In normal, frego bract, and nectariless cotton at four sites In the Western Cotton Growing Area, Tanzania, 1973-74. Site and trial Bwanga M w a m a l a M w a n h a l a U k i r i g u r u V a r i e t y Description IRG (73) 1a IRG (73) 1c IRG (73) 1d IRG ( 7 3 ) 1 e

Control (commer- U K 6 8 / U K 6 9 4 3 . 3 11.2 2 7 . 4 2 4 . 9 cial cultivar) m i x t u r e (100.0) ( 1 0 0 . 0 ) (100.0) ( 1 0 0 . 0 )

1 7 . 0 1 9 . 7 Frego bract U n s e l e c t e d 3 2 . 4 8-7 F 4 b u l k s of 7 8 . 4 ) 6 (77-7) (62.0) ( 7 9 . 1 ) 31.6 2 3 . 2 1 8 . 5 Nectariless f i r s t c r o s s t o 12.4 local varieties (73.0) (110.7) (84.7) (74.3)

SE ± 2 . 1 7 ± 0 . 9 7 ± 1 . 3 8 ± 1 . 6 7 S i t e m e a n 3 5 . 8 10.8 2 2 . 5 2 1 . 0 No. of weeks of counting 11 10 8 1 0

Source: Lee et al. 1975.

a . T h e v a l u e s q u o t e d a r e w e e k l y f l a r e d s q u a r e i n d i c e s , m e a n o f n w e e k s o f c o u n t i n g , l o w values indicate good resistance. b . Figures in parentheses are percentages of the control v a r i e t y .

3 5 7 Table 2. Bollworm resistance and other characteristics of normal, nectariless, frego bract, and glandless cott o n In an unsprayed trial at Ukiriguru, 1974-75.

C o r r e c t e d S e e d p e r F l a r e d s q u a r e f l o w e r G i n n i n g b o l l a b C u l t i v a r index count p e r c e n t a g e ( g )

c J 3 ( 7 2 ) 3 6 4 . 3 3 4 3 9 3 7 . 7 7 . 0 0 J 3 ( 7 2 ) 2 9 c 5 . 1 4 3 9 9 3 6 . 3 6 . 6 3 d S1 ( 7 2 ) 70 9 . 5 6 4 7 3 3 7 . 2 6 . 9 0 d B1 ( 7 2 ) 49 6 . 7 3 4 6 6 3 8 . 5 7 . 0 2 U K F r e g o ( 7 3 ) 1 1 1 . 5 7 3 7 6 3 6 . 7 6 . 7 8 U K F r e g o ( 7 3 ) 1 2 1 . 4 2 1 . 7 5 ± 0 . 5 1 6 3 7 1 3 6 9 ± 8 . 7 3 7 . 5 6 . 4 9 U K F r e g o ( 7 3 ) 1 3 2 . 5 6 3 5 9 3 9 . 4 8 . 1 8 U K Nec ( 7 3 ) 1 0 2 . 5 2 3 5 7 4 3 . 2 7 . 4 8 3 8 6 ± 8 . 7 U K Nec ( 7 3 ) 1 2 3 . 3 6 3 . 6 5 ± 0 . 5 1 6 4 1 2 3 8 . 8 8 . 2 0 U K Nec ( 7 3 ) 1 8 5 . 0 6 3 9 0 3 9 . 0 6 . 7 8 g l U K ( 7 3 ) 6 6 . 2 1 6 . 5 4 ± 0 . 6 3 1 3 3 4 3 6 3 ± 1 0 . 6 3 6 . 5 6 . 5 5 g l U K ( 7 3 ) 1 2 6 . 8 6 3 9 1 3 7 . 2 7 . 4 9 F r e g o x l o c a l 2 . 9 1 4 0 8 3 7 . 9 7 . 0 4

F 4 b u l k N e c t a r i l e s s x l o c a l 3 . 3 7 3 6 7 4 0 . 1 7 . 3 0

F 4 b u l k 6 . 6 3 U K - 6 8 C o m m e r c i a l 4 . 1 2 3 . 7 4 1 0 . 6 3 1 4 5 0 4 3 0 ± 1 0 . 6 3 6 . 3 U K - 6 9 v a r i e t i e s 3 . 3 5 4 1 0 3 6 . 0 6 . 5 5 S E t r e a t m e n t m e a n ± 0 . 8 9 3 ± 1 5 . 0 ± 0 . 3 2 ± 0 . 2 7 4

Source : Lee et al. 1975.

Correlation between flared square index and correcte d flower count was + 0.52, significant

a t 5 % . a. Low values indicate good resistance. b . Corrected for bollworm damage. c. Bollworm-resistant normal variety selected from 1 973-74 S.Z . Strain trial, Ukiriguru. d . Bollworm-susceptible normal variety selected from 1 973-74 S.Z. Strain trial, Ukiriguru.

Influence of Cropping Sequence February. However, a drought in January and on H. armigera Pest Status February adversely affected maize development and therefore the buildup of H. armigera. L o n g - Reed (1965) examined the role of maize in the duration UCA maize and some local varieties are buildup of H. armigera on cotton at and around sown in December and January and begin Ukiriguru. Apart from this work, no effort has been flowering in April, which coincides with flowering in made to examine the importance of the other late-sown cotton. cultivated crops in the population changes of H. The early-sown cotton season was prolonged in armigera. 1980-81 because of the delay in the second rainfall During the 1980-81 season, a start was made in peak; a top crop formed after the loss of the early identifying the cropping sequence at and around crop in mid-season drought. Ukiriguru in relation to alternative hosts of Heliothis Tomatoes are grown in backyard gardens and pest population changes. Crops studied throughout the year; however, farmers favor the included cotton, short- and long-duration maize, dry-season crop because it is less damaged by short-duration sorghum, chickpea, and tomatoes. diseases. This crop is considered a major The flowering pattern of these crops—i.e., the cultivated host for H. armigera. C h i c k p e a is a late- stages attractive to Heliothis—is shown in Figure 1. season crop, usually sown on residual moisture on Short-duration maize sown in October and early heavy (mbuga) soils. November started flowering mid-December and T h e level of Heliothis infestation on cotton was would have remained attractive until the end of regarded as being very low in the W C G A as a

3 5 8 whole. However, the results of sampling the different crops twice a week gave an idea of the level of infestation on each. The average larval counts per plant on unsprayed crops at flowering were: Katumani (short-duration maize) 0.12; cotton 0.014; UCA maize 0.11; sorghum 0.083; and chickpea 0.73. The infestation on chickpea was considerable.

Role of Natural Enemies in Controlling Heliothis

Reed (1965) reported that at Ukiriguru, the dry- season diapause breaks the association between Heliothis and most of its natural enemies, so that there is an uncontrolled rapid buildup of the pest on cotton early in the season. Reed also observed heavy parasitism and predation later in the season. However, with the changed farming system in which there is continuous cultivation of crops that have the ability to harbor Heliothis during the dry season, the predator-prey association may well have changed. Examination of the activity of adult Heliothis moths from light-trap catches at Ukiriguru, 1973 to 1980, showed that moth activity was continuous throughout the year, with two peaks. The major moth flight takes place towards the end of the main rainfall in April-May and the lower peak is in January. These two peaks are separated by a period of low moth activity during the dry season between June and October. To investigate pupal period and diapause, larvae collected in the field during the 1980-81 season were reared to pupal stage, and the pupal period observed (Table 4). There is some evidence, therefore, that even with a small percentage of diapausing population, continuous Heliothis activity throughout the year could support a small population of its natural enemies. Problems

Insecticidal Control

Acceptance by Farmers

About one-fifth of the cotton farmers in Tanzania spray their cotton, and about half of these apply an average of three sprays out of the six recommended. Those who spray often base their spraying on a scouting system, which is

3 5 9 Tomatoes

Infestation on early-sown chickpea

UCA long- duration maize flowering

Early-sown cotton flowering

Early-sown sorghum flowering

Early-sown short-dura• tion maize flowering

Dec Jan Feb Mar April May June July Aug

Figure 1. The flowering pattern of cotton, maize, sorghum, chickpea, and tomatoes in and around Ukiriguru, 1980-81 season. Arrows indicate period during which crop remains attractive to Heliothis. Table 4. Pupation period of field-collected larvae from different crops at and around Ukiriguru, 1980-81 season.

Range of A v e r a g e N u m b e r i n N u m b e r o f p u p a l d u r a t i o n d u r a t i o n diapause more than M o n t h p u p a e ( d a y s ) ( d a y s ) 30 daysa

J a n u a r y 7 2 11-17 14.5 0 February 2 3 14-16 15.2 0 M a r c h 53 12-25 17.6 0 A p r i l 3 5 15-42 1 6 . 5 1 May 44 12-19 15.2 0 J u n e 123 12-23 16.6 0 J u l y 168 14-32 17.7 1 A u g u s t 363 12-20 16.6 0

Source: Nyambo unpublished. a. According to Reed (1965) diapause duration in th e laboratory was 30 to 171 days after p u p a t i o n .

determined by the number of fully grown bollworms enemies. Reed (1965) reported about 27% and/or an increase in the number of flared squares parasitism of larvae collected from the field in the crop. A major disadvantage of this system is between March and July 1962 at Ukiriguru. Over a that by the time the farmer notices the bollworm similar period in 1964, after more intensive use of larvae, the damage has already been done to the insecticides, he observed only 6.4% parasitism on crop; additionally, larger d o s a g e s of insecticides larvae collected from the same crops. Reed are required to kill the full-grown larvae. expressed the fear that increasing use of insecticides at Ukiriguru might be reducing the activity of the natural enemies. This could be true Increased Insecticide Prices for TCA cotton seed production farms and research stations, where insecticides are used Insecticide prices are continuously rising, so that intensively, but may not be the case on farmers' even with government subsidies, cotton spraying is scattered plots. becoming less economic. In the 1974-75 season, a farmer needed to produce only 100 kg of seed cotton to pay for the cost of the insecticides, Weather whereas in the 1979-80 season, he needed 150 kg of seed cotton to pay for the same insecticide. The The continuous dry weather in January and problem of prices is more acute with the synthetic February in the WCGA, which has affected the pyrethroids. Although research has recommended buildup of H. armigera on cotton and its alternative some of them, it may be some time before they can host plants, has made the evaluation of Heliothis- be purchased cheaply enough for farmers' use. resistant plant material and scouting-based Moreover, some of the pyrethroids, particularly spraying unrewarding. cypermethrin and deltamethrin (decamethrin), have been observed to induce a red spider mite, Tetranychus spp, outbreak on research cotton Lack of Host-Crop plots. This is casting a shadow on the future of the Integration synthetic pyrethroids on cotton in Tanzania.

To date, Heliothis management on cultivated crops Effect of Insecticides on Natural Enemies has been considered in isolation on each crop. Control efforts have been concentrated on An increased reliance on insecticides could have a particular crops only, ignoring the fact that t h e detrimental effect on Heliothis armigera natural different crops in the system could play an

361 important part in increasing or decreasing Heliothis this Workshop. I would also like to acknowledge pressure on others. The cropping sequence could permission to present the paper, given by the be better utilized to facilitate integrated Heliothis Director, Tanzania Crop Research. management.

Future Work References

Heliothis management in Tanzania warrants more BROWN, K.J. 1962. A g r o n o m y a n d c r o p p h y s i o l o g y intensive research for a number of reasons. First, progress report, 1960-61. Experiment Stations, Empi r e our farming system is being changed from small, Cotton Growing Corporation, Tanganyika Lake Province, isolated fields in scattered villages to large, Tanganyika. 8 pp. organized communal villages (ujamaa villages) HACKETT, D.S., and KABISSA, J.C.B. 1980. P a g e s and block farms, where both food and cash crops 7 - 8 in Cotton research annual report, 1979-80. Tanzania: receive equal importance. The pest pressure under Agricultural Research Institute, Ukiriguru, Mwanza. such a farming system is likely to be more severe. LEE, B.J.S., WALTON, I.C., JACKSON, A.C., S e c o n d , Heliothis control has so far been centered MARANDU, W.Y.F., and KAPINGU, M.P.K. on single crops, without taking into consideration 1975. Pages 26-56 in Annual report, 1974-75. Tanzania: the agroecosystem as a whole. Some of the Agricultural Research Institute, Ukiriguru, Mwanza. cultivated food crops will be a potential source of REED, W. 1965. Heliothis armigera in W e s t e r n T a n g a - infestation or a reservoir of natural enemies for nyika, Parts 1 and 2. Empire Cotton Growing Corporation other crops in the cropping sequence. Third, research memoirs 61, Tanganyika. Heliothis control to date has largely depended TREEN, A.J. 1979. U k i r i g u r u c o t t o n r e s e a r c h . I n A n n u a l upon insecticides; in view of the problems often report 1978-79. Tanzania: Agricultural Research Institute, associated with a heavy reliance on insecticide Ukiriguru, Mwanza. use, there is need to search for more efficient, mo r e reliable, and cheaper control measures. TREEN, A.J. 1980. Entomology (WCGA). I n U k i r i g u r u cotton research annual report 1979-80. Tanzania: Agri• With these limitations in mind, a research cultural Research Institute, Ukiriguru, Mwanza. program has been initiated to study the following a s p e c t s : TREEN, A.J. 1981. Cotton entomology (WCGA— • The effect of the changing farming system on the Ukiriguru). Summary of 1980-81 results. Ukiriguru Agr i • occurrence of Heliothis, with particular reference cultural Research Institute, Mwanza, Tanzania. to its abundance and the damage it can cause to cultivated crops. • Heliothis key mortality factors on the major field crops. • The establishment of a monitoring and forecasting system, including the use of simple traps. • Chemical control of Heliothis with emphasis on selectivity against non-target organisms, including the evaluation of more efficient and safer insecticides.

Acknowledgments

I wish to thank Mr. George B. Jones, the Tanzania Cotton Research Coordinator, for reading the draft, his encouragement and useful criticism in preparing this paper, and Dr. J.C. Davies, Director of International Cooperation, ICRISAT, for the invitation and for funds enabling me to participate in

3 6 2 Progress in Research and Development for Heliothis Management in the Sudan

Ahmed Nasir Balla*

Abstract

The change in the status of Heliothis armigera from an occasional and sporadic cotton pest to a major problem under Sudan Gezira conditions is associated with changes in crop rota• tions and the increased area under crops that serve as host plants for the pest. Groundnut growing early in the season over a large area has provided the insect with a suitable host plant on which to develop prior to cotton infestation. Development of Heliothis infestation on sorghum coincides with the start of cotton infestation and therefore contributes to later attacks on cotton. Advancing the sowing date and planting of early-fruiting cotton varieties disposes the cotton to H e l i o t h i s attack. At present, the strategy for Heliothis management is based on the use of insecticides to keep the early bollworm damage below the economic threshold. Emphasis is placed on the use of insecticides that interfere least with natural control agents. Programs tor developing pest-resistant cotton varieties are under way.

The American or African bollworm (Heliothis was only occasionally and sporadically infested. armigera) has been recognized as a pest of cotton Serious infestation in the Gezira was reported dur• in the Sudan since organized cotton production ing the 1931-35 seasons by Cowland, and the started in the country. Reports of the then Agricul• 1951 -54 seasons by Joyce. However, in these sea• tural Research Corporation contain numerous sons of high infestation, the distribution of the pest records of this pest from different parts of the co u n • was not uniform, varying with locality and generally try where either rainfed or irrigated cotton was culti• associated with the early-sown crop. In the early vated (Cowland 1931-35; Bedford 1934-38; Joyce 1960s, however, a marked change took place and 1949-54). Heliothis armigera then was a major pest Heliothis established itself as a major pest. This in the central rainlands and the inland deltas (Tokar change was at first confined to the southwest and Gash Deltas), but in the Gezira irrigated cotton (Managil) extension but later spread to the whole Gezira. The importance of Heliothis has progres•

*Entomology Section, Gezira Research Station, ARC, Wad sively increased with time and currently it consti• Medani, Sudan. tutes, together with the cotton whitefly, Bemisia

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management 15-20 November 1981, Patancheru, A.P., India 3 6 3 tabaci, the major hazard to the irrigated cotton crop intensified and diversified rotation from the very in the Gezira. On the other hand, the pest continue d beginning. So the original rotation cotton-ground- to command its traditional major status in rainfed nut/lablab-sorghum-fallow-cotton-fallow had both cotton. cotton and groundnut as major cash crops. In 1967, wheat was added, and the rotation was modified to: cotton - sorghum fallow - cotton - wheat - Crops and the Cropping groundnut/lablab. In the mid-1970s the fallow was eliminated, and the rotation was changed to: Systems in the Gezira cotton - wheat - groundnut / vegetables / sorghum / fodder. The Gezira Scheme, which was launched in 1925, has witnessed several changes in the spectrum of crops grown, the crop rotations adopted, and the Changes in Areas Under total acreage sown to each crop. These changes were dictated by economic considerations, devel• Different Crops opment of plant diseases, and other practical rea• The main rotational crops that cover sizable areas sons. The major changes are summarized below. are cotton, groundnut, sorghum, and wheat; the first three of these are host plants, of Heliothis. T h e Changes in Crop Rotations cotton area increased progressively from 80000 feddans (33600 ha) in 1925 to reach about a quar• The first rotation adopted in the old Gezira was: ter of a million (105 000 ha) by 1957-58 (Table 1). cotton - sorghum / lablab - fallow. in 1931, and in view With the completion of the Managil Extension in the of the spread of leaf curl and bacterial blight dis• 1962-63 season, the total area under cotton was eases on cotton, the legume, Dolichos lablab was doubled. abandoned, and the rotation changed to: cotton- fallow - sorghum - lablab - fallow - cotton - fallow - fallow. The main feature of these early rotations is the emphasis on cotton as the major crop, and the Table 1. Area (ha) under cotton, sorghum, and ground - large proportion of land left fallow to combat cotton nut in the Sudan Gezira over three decades—1941-42 diseases and renew soil fertility. to 1972-73. In the early 1960s, a new policy of crop diversifi• cation was implemented, and groundnut was intro• S e a s o n C o t t o n S o r g h u m G r o u n d n u t duced commercially as a second major cash crop besides cotton, after it had shown its suitability for 1 9 4 1 - 4 2 8 7 0 7 1 6 4 4 2 8 the heavy Gezira clays. At the same time, wheat 1 9 4 6 - 4 7 8 6 6 7 4 4 3 4 6 7 was also introduced as a cash crop. Consequently, 1 9 5 1 - 5 2 9 2 8 8 5 4 6 5 3 5 1 1 6 7 1 9 5 6 - 5 7 1 0 3 1 0 4 5 1 5 5 7 4 0 3 two different rotations were followed: one for the 1 9 6 2 - 6 3 2 0 3 5 7 1 9 5 0 2 8 1 0 0 1 5 southern Gezira where the rotation became cotton- 1 9 6 7 - 6 8 2 3 2 6 3 8 1 3 2 1 9 1 4 2 7 1 5 groundnut/lablab-sorghum-fallow-fallow-cotton- 1 9 7 2 - 7 3 2 4 7 7 7 2 1 2 3 5 2 0 7 4 7 3 8 fallow-fallow. In the northern Gezira, wheat was introduced, and here the rotation adopted was: cotton-lablab/fallow-sorghum-fallow-fallow-cotton- wheat-fallow. Though these newly adopted rotations had two new cash crops besides cotton, the large During the decade 1948-1958, the area annually proportion of fallow remained. In the mid-1970s, with sown to groundnut was very low. With the start of the launching of a policy of crop intensification, the the Managil Extension this area began to expand areas left fallow were drastically reduced, and the rapidly; at present, groundnut area is over a quarter rotation adopted in the old Gezira became cotton- of a million feddans (105000 ha). wheat - groundnut / sorghum / vegetables / rice / f o d - Few changes occurred in the sorghum areas in der-fallow. the Scheme during the 1940s and 1950s, but in the In the southwest (Managil) extension, which was early 1960s, the sorghum area increased to about a started in 1957 and developed in phases to be quarter of a million feddans and is now approach• completed by 1962, the plan was to implement an ing 300 000 feddans (126000 ha) in the 1980s.

364 Heliothis Infestations val numbers per head were found to vary, but as on the Rotational Crops many as 30 larvae per head or more were encoun• tered in some seasons. Loss in grain due to Helio• The sequence of cropping starts with groundnut, this damage is estimated as 5 to 10%. From a study followed by sorghum, then cotton, and lastly wheat. of sorghum infestation, Topper (1978) concluded This sequence satisfied the optimum requirements that only one generation develops on the crop in of the crops included in the rotation and avoids the the Gezira and the adults produced oviposit on overlap of the various cultural operations. cotton during the first half of October.

Cotton Groundnut

The Gezira area grows predominantly long-staple The cultivar grown commercially is Ashford, which cotton (Gossypium barbadense); however, in takes about 140 days to mature under the Gezira recent years, medium-staple cotton (Gossypium conditions. The crop is sown in early June and hirsutum) varieties traditionally grown outside the harvested in November. Gezira were introduced. These varieties are deriv• Heliothis larvae feed on groundnut leaves, young atives of the American Upland Acala and they are leaves being preferred to older leaves. Laboratory potentially higher yielders than the long-staple breeding has shown that larvae develop normally ones. The area under medium-staple cotton is on young leaves but they suffer high mortality when about 12% of the total cotton area in the current bred on old leaves. Economic losses resulting from 1981 -82 season. Heliothis feeding on groundnut are negligible. Long-staple cotton used to be sown from mid- A study of Heliothis infestation on groundnut in August to late-August. However, in the 1970s, the the Gezira Research Farm, showed low popula• sowing date was advanced by about 2 weeks. This tions during the period August to October, with a was made possible by the breeding of varieties peak (1.9 larvae/50 random plants) occurring in resistant to the bacterial blight disease caused by late August, then declining to 0.2 larvae per 50 Xanthomonas malvacearum, which was the major plants by mid-September (Balla 1968). In a similar factor preventing earlier sowing. Early sowing study in the Managil Extension during 1970, it was leads to higher yields and better grades of cotton. found that the infestation was higher, but again a Heliothis larvae feed on the fruiting points of the peak of 5 larvae per 50 plants was attained towards cotton plant, i.e. flower buds, flowers, and bolls a n d the end of August. Topper, in an intensive study of the start of infestation is associated with the start of Heliothis on groundnut in 1976 and 1977, found the fruiting cycle. Advancing the sowing date that the numbers of larvae increased from July until results in earlier fruiting and consequently earlier September, with a pronounced peak in late August- bollworm attack on cotton. early September, after which the numbers declined The growth pattern and fruit initiation vary in the in October (Topper 1978). He showed that the lar• two types of cotton grown in the Gezira. Given the val peaks correspond to adult moth peaks that later same agronomic treatments, the long-staple cot• oviposit on cotton in early September to mid- ton takes 80 days from sowing to the first flower, October. produced on the 15th to the 18th node. For the Acala type, the first flower is produced on the third Sorghum (Dura) to fourth node after 50 days from sowing (Far- brother 1973). It follows, therefore, that infestation Heliothis larvae feed on sorghum grain at the milk in Acala types of cotton is earlier (early September) stage only but after that stage sorghum infestation compared with the long-staple varieties (about ceases. It was observed that compact-head varie• mid-September). ties, which predominate in the Sudan, are more heavily infested than open-headed varieties. In the Impact of Insecticides on Gezira, several local and improved varieties are grown under irrigation. The crop is sown in early Natural Control Agents July, and the milk stage under the Gezira conditions is attained normally during the early September to Heliothis larvae are parasitized by some ten differ• mid-October period, depending on the variety. Lar- ent species in the Sudan (Table 2). The incidence

3 6 5 T a b l e 2 . H e l i o t h i s armigera parasites and predators T a b l e 3. P e r c e n t a g e p a r a s i t i s m in Heliothis in the a In the Sudan. Sudan Gezira.

P a r a s i t e s : S e a s o n S e a s o n 1 9 3 3 - 3 4 1 9 6 5 - 6 6 Euplectrus laphygmae F e r r . ( C o w l a n d ) (Lazarevic) Drino imberbis W e i d . Exorista s p p . O c t o b e r 2 - 4 0 Isomers cinerascens R o r d N o v e m b e r 6 - 1 2 0 Sturmia inconspicua M g n D e c e m b e r 0 - 5 0 Hypeuchalcidia soudanensis S t e f f J a n u a r y 3 4 - 3 7 0 Che tonus versatilis W i k n F e b r u a r y 5 3 1 Meteorus laphygmarum B r u e s M a r c h 3 9 Elasmus johnstoni F e r r Goniophthalmus halli Pediobius furvum G a h Cardiochiles sp Microbracon kirkpatricki Our continuous monitoring for parasites during the P r e d a t o r s : 1970s and 1980s in the Managil and Gezira has Eumenes maxillosus De G e e r shown that the incidence has declined to almost nil. Chrysopa carnea S t e p h a . C o m p i l e d b y B a l l a a n d A h m e d ( 1 9 8 1 ) . The Strategy of Heliothis Control in the Sudan of larval parasitism in the bollworm was recorded At present, the use of insecticides is the only con• by Cowland during the season 1933-34 before trol method resorted to in combating Heliothis. insecticide application was started in the Gezira. Though other rotational crops including groundnut He found that larval parasitism, which was low in and sorghum are attacked and contribute to the October, increased progressively reaching a peak infestation on cotton, control is confined to the of over 50% by February (Table 2). cotton crop only. Several insecticides have been Cotton spraying in the Gezira started in the 1944- tested in the Sudan, approved, and registered for 45 season on a limited area, using tractor-mounted commercial application against the American boll- sprayers with DDT, primarily for the control of the worm. They are either emulsifiable concentrates, cotton jassid Empoasca lybica de Berg. During the wettable powders, water-soluble concentrates for 1950s, aerial application replaced ground applica• low-volume spraying, or oil-based formulations for tion, and the number of sprays increased to an ultralow-volume application. The American boll- average of two sprays applied in midseason, with worm is usually found in association with other DDT still the main insecticide in use. In the early pests, particularly whitefly, and since few chemi- 1960s, the American bollworm and whitefly started cals control the two pests when used singly, the to increase, requiring three to five sprays. DDT an d rule is to use mixtures of chemicals (ready mixtures dimethoate were the main chemicals used, usually or tank mixtures) to combat the pest complex. as a mixture, to control the pest complex. In the late These mixtures also undergo screening tests for 1960s and early 1970s, the whitefly became a more compatibility and efficacy. serious pest, requiring five to seven sprays annu• Proper timing and prompt action are critical for ally. Several insecticides were applied, but DDT still the control of a pest like Heliothis. Insecticide appli• d o m i n a t e d . cation when the majority of larvae are at an early The adverse impact of increased spraying on stage of development ensures a good kill and pre• parasites and predators is well established. During vents extensive d a m a g e . This is a c h i e v e d by taking the 1965-66 season, Lazarevic studied the inci• Heliothis egg counts on the crop. The presence of d e n c e of Heliothis parasitism in the Managil Exten• eggs is also indicative of the presence of oviposit• sion and found that there was a general decline ing females, which are consequently killed by from the peak (39%) attained in March (Table 3). insecticide application. The economic threshold at

3 6 6 which the spraying operation commences is 10 FAO/UNEP African program for the development eggs and larvae per 100 random plants. and application of integrated pest control in cotton.

Research and Development in Discussion and Conclusions

Heliothis Management Heliothis armigera is a polyphagous insect pest that feeds on several cultivated plants and weeds Though the strategy ot control developed for Helio- in the Sudan (Balla 1978). Though it is found all the this in the Sudan proved to be effective in minimiz- year round, it is more abundant during the period ing losses to the pest.the need arose to revise this August-October. Under natural conditions the strategy along the lines stipulated for the develop- buildup starts as early as June on weeds that grow ment of an integrated control program for the with the advent of the rainy season. The fast- cotton-pest complex as a whole. This need has growing weed, Ipomoea cordofana (Convolvula- become pressing in recent years, in view of the ceae) is particularly noted for the high incidence of increased importance of the cotton whitefly. Helio• Heliothis larvae. The survival of these early popula• this is the major pest attacking cotton early in the tions is important for the future development of the season, preceding the whitefly, and the first sprays peak populations during August-October. Since applied are primarily directed towards it. It is infestation on long-staple cotton starts in early or believed that the aggravation of the cotton whitefly mid-September, i.e., during the peak period of the is partly due to the disruptive effect of these early seasonal occurrence of Heliothis, factors affecting sprays of persistent, broad-spectrum insecticides the survival of the early populations in turn deter• such as DDT on the parasites and predators of mine cotton infestation. The major factor determin• Bemisia tabaci (Eveleens and Abdel Rahman ing the size of these early populations is the 1979). abundance of weed host plants, which is governed Delaying the first spray so as to decrease the by the distribution and abundance of rainfall. If the early insecticide pressure on the parasites and rainfall pattern is such that weed growth is abund• predators was found to predispose the crop to eco• ant during June-July, the bollworm populations are nomic losses in yield as a result of Heliothis d a m • large; consequently, later infestations on cotton are age (Eveleens et al. 1981). Thus, to protect the cr o p heavy, and vice versa. This perhaps explains the from early bollworm damage, insecticide use sporadic and occasional nature of the pest occur• appears indispensable at the present time. How• rence in the Gezira prior to the 1960s. Rainfall in ever, to minimize the adverse effect on the paras• this region varies from season to season; on the ites and predators, it has become necessary to aim other hand, in the Central Rainlands, the annual at selecting insecticides that interfere least with the rainfall is higher, and sufficient weed growth is buildup of these natural control agents. The recent present annually for bollworm development. stoppage of DDT, which is a broad-spectrum, per- In the early 1960s, the introduction of groundnut, sistent chemical of long standing in the Sudan, is a a host plant of Heliothis, under irrigation in the step taken partly to achieve this end. At present, Gezira and the subsequent expansion in its work is in progress to evaluate the impact of other acreage have provided the pest with the needed chemicals on parasites and predators. Microbial host plant early in the season; thus the annual Insecticides, such as Bacillus thuringiensis a n d fluctuations corresponding to the rainfall have polyhedral viruses, which have shown some prom• been evened out. The fact that the Heliothis out• ise under Sudan conditions hitherto, are being break was initially experienced in the Managil investigated. Extension, where groundnut was introduced in the Breeding for bollworm resistance in cotton has rotation, is perhaps further evidence for the assoc i • long been recognized as an important approach in ation of Heliothis with groundnut. However, pest management. Earlier attempts were unsuc• although the American bollworm is now an impor• cessful, and the efforts were consequently aban• tant annual pest in the Gezira, it is more serious in doned. Interest in this line of research has been some seasons than in others, reflecting the varia• revived lately (Balla and Khalifa 1980). More tion in rainfall amount and distribution that still recently, the work on breeding pest-resistant cot• operates. ton varieties has been expanded under the While groundnut provides a host plant for Helio-

3 6 7 this development prior to cotton infestation, FARBROTHER, H.G. 1973. G e z i r a R e s e a r c h Station sorghum is infested at about the same time as a n d S u b s t a t i o n a n n u a l report, 1 9 7 2 - 7 3 , W a d M e d a n i , cotton. The single generation developing on S u d a n .

sorghum produces adults that oviposit later on cot• JOYCE, R.J.V. 1950-1954. Agricultural R e s e a r c h Div• ton. Expansion in sorghum area has thus also con• ision Sudan, Annual Reports 1949-50,1950-51,1951 -52, tributed to the increased cotton infestation. 1952-53,1953-54, Wad Medani, Sudan. As mentioned earlier, the bollworm is seasonally LAZAREVIC, B.M. 1966. A g r i c u l t u r a l R e s e a r c h D i v • more abundant during August-October. Therefore ision, Sudan, Annual Report 1965-66. with regard to cotton, practices like advancing the TOPPER, C. 1978. T h e i n c i d e n c e of H. armigera larvae sowing date that result in exposing the crop for a a n d adults o n g r o u n d n u t s a n d s o r g h u m a n d t h e p r e d i c t i o n prolonged time in this period, will subject it to heavy of oviposition on c o t t o n . P r e s e n t e d at t h e T h i r d S e m i n a r bollworm attacks. Similarly, cultivation of early- on the Strategy for C o t t o n Pest C o n t r o l in the S u d a n , flowering varieties, such as the short- and medium- CIBA-GEIGY, Basel, Switzerland. staple cottons, leads to heavier bollworm attacks. Though the role of parasites, which appear to be the dominant natural control agents in the Gezira, is limited early in the season, they increase progres• sively, as shown by Cowland's studies, before the use of insecticides. The increased frequency of sprays and the use of persistent broad-spectrum chemicals have adversely affected the parasites. Attempts to use less destructive chemicals and alternative methods of control such as pest- resistant cotton varieties would lead to the restora• tion of these beneficials—parasites and predators not only of Heliothis but of other pests—and to the reduction of the number of sprays needed.

References

BALLA, A.N. 1968. Gezira R e s e a r c h S t a t i o n a n d S u b - stations Annual Report, 1967-68, Gezira, Sudan.

BALLA, A.N. 1978. S t u d i e s o n t h e A m e r i c a n b o l l w o r m H. armigera in t h e S u d a n G e z i r a . P r e s e n t e d at the S y m p o • s i u m o n C r o p Pest M a n a g e m e n t i n the S u d a n , 1978.

BALLA, A.N. and KHALIFA, H. 1980. Gezira R e s e a r c h Station and Substations annual report, 1979-80, Gezira, S u d a n .

BEDFORD, H.M. 1935-1938. Agricultural Research Division, annual reports, Wad Medani, Sudan.

COWLAND, J.W. 1931-1935. Agricultural Research Division, Sudan, annual reports, Wad Medani, Sudan.

EVELEENS, K.G., and ABDEL RAHMAN, A.A. 1 9 8 0 . T h e c o t t o n whitefly p r o b l e m : c a n the tide b e t u r n e d ? P r e s e n t e d a t t h e 4 4 t h M e e t i n g o f the N a t i o n a l Pests and Diseases Committee, Working Paper No. 5, November 1980, Wad Medani, Sudan.

EVELEENS, K.G., BALLA, A.N., and ABDEL RAH• MAN, A.A. 1981. Report p r e p a r e d for t h e 4 5 t h M e e t i n g o f the National Pests and Diseases Committee, November 1981, Wad Medani, Sudan.

368 The Problems and Prospects of Heliothis Management in Southwest Asia

G. Hariri*

Abstract

The most important crops that are attacked by Heliothis spp in southwest Asia are cotton, tomatoes, tobacco, chickpeas, and maize. H. armigera (Hb.) is widely distributed in the region and causes severe damage in Turkey, the northern provinces of Iran, and in some areas of other countries in the region. Second in importance is H. viriplaca (Hutn.). which is causing severe damage in Iran and seems to be important in Syria also.

The Southwest Asia region is characterized by dif• Status of Heliothis ferent climatic zones. The interaction of altitude, Species in the Region latitude, and distance from the Mediterranean, Black, and Caspian seas and the deserts of the Any evaluation of pest damage to crops in the Arabian Peninsula has led to the evolution of differ• region is of a temporary nature, because of the ent agroclimatic subregions. Accordingly, the changes in the standard of living of farmers and in amount and distribution of rainfall in late autumn, agricultural practices, such as crop rotation, inten• winter, and early spring determine the growing peri• sity of cropping, expansion of land under irrigation, ods of rainfed crops in the high plateau (Turkey, mechanization, introduction of new crops, and land northern Iran, and northern Iraq) and lowland reclamation. With the increase in irrigation facilities (Syria, Lebanon, Jordan, and Palestine) areas of in vast areas, continuous cropping became possi• the region. The rainy season is followed by several ble during summer, and this has resulted in the months of dry summer. buildup of populations of polyphagous insect pests. There are two types of rotations under rainfed The most important crops attacked by Heliothis conditions; each has its winter and summer crops. spp in the region are cotton, tomatoes, tobacco, Cereals (wheat and barley) and winter legumes chickpea, and maize. The data on area and pro• (lentils, faba beans and vetches) are grown in win• duction of these crops are given in Table 1. Four ter. Sorghum, sesame, watermelon, and chickpeas Heliothis species are recorded in the region attack• are grown in spring. Summer legumes (beans, ing these main and other host crops (Table 2). H. cowpeas, peas, groundnut, and soybeans), maize, armigera (Hb.), H. viriplaca (Hufn.), H. peltigera cotton, tomatoes, and other crops are grown under (Denis & Schiff.) and H. nubigera H.-S. Of these, H. irrigation as summer crops. Irrigated crops are armigera is the most widely distributed in the region grown along the riverbeds of the region; surface and is known to cause severe damage in Turkey, and artesian wells are also commonly used for the northern provinces of Iran, and some areas of irrigation of summer crops. Syria, Lebanon, and Palestine', and moderate

*University of Aleppo, Aleppo, Syria. 1. Israel.

T o m a t o e s T o b a c c o C h i c k p e a s M a i z e Cotton Lint C o u n t r y A P A P A P A P P

T u r k e y 108 3 5 0 0 2 6 0 230 200 250 550 1150 481 Syria 30 4 6 0 13 13 21 70 31 7 0 127 L e b a n o n 6 7 5 8 5 1 2 2 2 J o r d a n 10 172 3 1 3 2 P a l e s t i n e 5 258 1 1 4 4 3 13 7 8 Saudi Arabia 16 167 3 4 North Yemen 6 6 6 4 9 5 2 South Yemen 1 2 6 15 4 United Arab Em i r a t e s 1 23 B a h r a i n 10 K u w a i t 1 11 I r a q 41 457 12 11 15 9 35 6 5 7 Iran 28 3 2 6 13 15 39 43 4 2 6 0 7 0

T o t a l 246 5 4 5 9 317 284 2 8 3 3 8 0 736 1474 7 6 9

S o u r c e : F A O ( 1 9 8 1 )

damage in other countries of the region. Second in 1970-71 (Barbulescu 1973). The damage by H. importance is H. viriplaca, which has been reported armigera in tomato in the Aegean area (Turkey) causing severe damage in Iran and seems to be was estimated to be as much as 36% (Ongoren et important also in Syria (Table 2). al. 1977). H. armigera may be a threat to cotton, which is one of the most important cash crops in some countries of the region, especially when it is grow n Population Buildup together with tomato, maize, or chickpea regularly. The insect switches over from these crops and Three important factors are involved in Heliothis becomes serious on cotton. In small areas in west• population buildup in the region. The first is the ern Syria and northern Lebanon, where cotton is growing of suitable hosts, together or in sequence. grown together regularly with corn, infestation may Damage to cotton in Syria depends on other early reach 100% (Talhouk 1969). But in other major crop hosts on which there is buildup of populations cotton-producing areas of Syria, infestations rarely that move to cotton as these hosts become unat• reach up to 10%. Peyrelongue (1966) estimated tractive. H. armigera is more important in the areas infestation during the 1960s at 7%. Recent estima• growing chickpeas, maize, and tomatoes together tions of H. armigera infestation on cotton show that regularly with cotton. The second factor in moth there is an increase in the importance of Heliothis population buildup is related to the migratory habit as a destructive pest in some fields, which may be of H.armigera as well as H. viriplaca, H. peltigera, due to late planting or to the increase in chickpea a n d H. nubigera (Rivnay 1962; Wiltshire 1957). In area (Elmosa 1981). certain instances, the moths may fly to the region Crop loss estimations in the region vary from from the warmer parts of Africa, thus reinforcing the year to year and are inadequate in some countries. resident local populations (Talhouk 1969). Crops Reports on H. armigera being a major pest and sown in virgin lands in the semidesert of the Negev causing loss in many crops in Iran indicated that were heavily attacked by migrant Heliothis, w h i c h damage in field-grown maize ranged from 8 to 55% was never known there before (Rivnay 1962). Thus in 1968 and 3 to 46% in 1969, but was only 1 % in the invasion by Heliothis may occur as a result of

3 7 0 Table 2. Heliothis spp.a a n d h o s t c r o p s i n s o m e c o u n t r i e s o f s o u t h w e s t A s i a .

S a u d i S o u t h C r o p T u r k e y S y r i a L e b a n o n J o r d a n P a l e s t i n e A r a b i a Y e m e n I r a q I r a n

T o m a t o HA***b HA**b , HN*b HA* H A * * , H P * HA** H A * H A * * HA* H A * , H V * * T o b a c c o HP* H A * , H N * HA** HA**, HP* HA**, HP*, HV** HN** HP** E g g p l a n t HN* G r e e n p e p p e r HA* HA* HA** HA* C h i c k p e a HA**, HV**, HA**, HP* ?HA* HP* HV* HP* HV** P e a . HA** H V * , H A * L e n t i l HA*, HV*. HP* HV* G r o u n d n u t HA** A l f a l f a HA", HP*, HA* H A * , H V * HN* C l o v e r HA** Melon, cucumber. a n d s q u a s h HA* C o t t o n HA*** HA* H A * * , H P * HA* HA**, HA*",HP*,HV" HP* HP* O k r a HA* M a i z e HA* HA** HA** H A * . H V * S o r g h u m HP* HP* HV* F l a x HV*** B e e t s HA** ?HA* HP* H A * , H V * S u n f l o w e r HP* HA* HA* S a f f l o w e r H A * * , H P * H N * * , H P * * C a b b b a g e HA** C a r n a t i o n HA** C i t r u s HA** G r a p e HA*

References: Turkey-lleri 1960. Gentry 1965, Ongoren et al. 1977; Syria-Gentry 1965, Talhouk 1979, Barbandy 1973. Hariri 1972.1979; Lebanon-Gentry 1965, Talhouk 1969; Jordan-Gentry 1965, Elmosa 1979; Palestine-Bar 1979, Rivnay 1962, Gentry 1965; Saudi Arabia—Martin 1977; South Yemen—Ba-Angood 1977; Iran—Gentry 1965,Zahedi 1968, Barbulescu 1973,Mor a d e s h a g i and Poormirza 1976; Iraq-Wiltshire 1957, Gentry 1965, Selim 1977.

a . H A = H e l i o t h i s armigera; H N = H . nubigera; H P = H . peltigera: H V = H . viriplaca.

b . Infestation level: "'severe, control measures essential; "moderate, control measures needed occasionally or locally; *tow, control measures seldom needed. the long-distance movement from one area to Monitoring and Future Needs in another as well as from one crop to another. The Management Research third factor is the introduction of new crops on a Heliothis large scale, which gives excellent possibilities for A review of the literature revealed a lack of basic mass development of Heliothis, which might have information on the biology and ecology of Heliothis formerly been of minor importance (Bytinski-Salz spp in most countries of the region. Currently there 1965). are studies in progress to determine the injury thre• Other factors are also important in the buildup of sholds for Heliothis as well as other main insect moth population. A mild winter or any early spring pests of cotton and the role of natural enemies in allows the moths to emerge from diapaused pupae controlling them (Stem and Sabek 1981; Elmosa in February-March (Hariri 1979). Chickpea plants 1981), and in chickpea fields (ICARDA, unpub- at seedling stage are attractive to Heliothis spp lished). The economic threshold of H. armigera on egg-laying moths, and so could act as an early cotton in Egypt was determined as 10 young lar- build-up host for these pests; this is in contrast to vae/100 plants. other crops, where egg-laying is known to occur Due to the increase of maize cultivation in Azer- only during the flowering and fruiting periods (Sith- baidzhan (USSR), the economic injury threshold for anantham et al. 1981). In cotton fields, the moths H. armigera on cotton has been revised to 5 to 6 start to appear as early as June (Barbandy 1973). larvae and 10 to 12 eggs of the first generation and In a recent study carried out at the ICARDA site 10 to 12 larvae and more than 20 eggs of the in North Syria during the 1980 and 1981 growing second generation per 100 plants, with some differ• s e a s o n s , H. armigera adults were caught in chick- ences in these figures in different areas (Mamed- pea and cotton fields in pheromone traps. The moth ova 1978; Mamedova et al. 1975). catch increased steadily from February to July in For future Heliothis management research in the chickpea fields, while it declined from July to region, the following topics are suggested: November in cotton fields, and few moths were caught in December. The catch in cotton was ten a. Further work on the evaluation of crop loss times greater than in chickpea fields (ICARDA, and economic damage threshold of Heliothis unpublished). Light traps in chickpea fields from in each country of the region. April to June 1981 indicated that H. viriplaca moths were more abundant than H. armigera or H. peltig- b. Emphasis on the use of insecticides in inte• era. Moths emerged from pupae collected from grated control of Heliothis spp and careful chickpea and lentil fields during the 1980 and 1981 monitoring of the development of insecticide seasons showed that H. armigera w a s more resistance. abundant in the 1980 season than the other two c. Work on determining the role of natural ene• species, whereas H. viriplaca was more abundant mies, such as parasites and specific dis• in the 1981 season (ICARDA, unpublished). eases, and their possible use against Little is known about the role of natural enemies Heliothis spp. in suppression of Heliothis spp populations in the Southwest Asia region. Recorded' principal paras• d. Further studies on the biology and population ites of H. armigera larvae were Hyposoter didyma- dynamics of Heliothis spp using an efficient tor (Thnb.) Meteorus sp, a n d Bracon hebetor Say. trapping system. H. didymator was a significant limiting factor of H. armigera populations on cotton (Bar et al. 1979). In Turkey, B. hebetor was found parasitizing H. armig• era larvae on tomatoes (Ongoren et al. 1977), while References in Syria, Habrobracon brevicornis W e s m . w a s BA-ANGOOD, S.A.A. 1977. C o n t r o l o f the t o m a t o fruit- found parasitizing larvae of H. armigera a n d Earias w o r m , Heliothis armigera Hb. (Lepidoptera: Noctuidae), in insulana Boisd. on cotton (Stam and Sabek 1981). People's Democratic Republic of Yemen. Journal of Ho r • The bacteria, Bacillus sp a n d Hafnia sp w e r e ticultural Science 52: 457-459. recorded infecting H. armigera larvae (Ongoren et BAR, D., GERLING, D., and ROSSLER, Y. 1979. B i o • al. 1977). The predators of eggs and larvae of H. nomics of the principal natural enemies attacking Helio• armigera w e r e Orius spp a n d Chrysopa carnea this armigera in cotton fields. Environmental Entomology Steph. (Bar et al. 1979). 8: 468-474.

372 B A R B A N D Y , A . R . 1 9 7 3 . C o t t o n i n s e c t s i n Deir Elzor era Hb.) harmful on t o m a t o e s in A e g e a n region. Bitki Governorate. Ministry of Agriculture Agrarian Reform, H o r u m a Bulteni 17: 3 - 2 8 . Syria, Leaflet 4 0 , 32 pp. (In A r a b i c ) . P E Y R E L O N G U E , J.Y. 1966. Rapport d e m i s s i o n e n B A R B U L E S C U , A . 1973. S o m e o b s e r v a t i o n s o n the Syrie. Cotonnier entomologie. Internationale Recherche biology, e c o l o g y a n d a t t a c k of Heliothiszea B o d d i e ( L e p i - Cotonnier Tropicale, Paris, France. 71 pp. d o p t e r a ) in t h e c o n d i t i o n s of Rasht (Iran). P r o b l e m s de R I V N A Y , E. 1962. Field c r o p pests in the N e a r East. T h e Protectia Plantelor 1:311 - 3 1 7 . C i t e d in R e v i e w of A p p l i e d H a g u e , Netherlands: J u n k Publishers. 4 5 0 pp. Entomology Series A 63: Abstract 1931. S E L I M , A.A. 1977. Insect pests of safflower (C a r t h a m u s B Y T I N S K I - S A L Z , H . 1965. Effects o f m o d e r n a g r o t e c h - tinctorius) in Mosul, Northern Iraq. M e s o p o t a m i a J o u r n a l nical methods on the agricultural insect pest population. In of Agriculture 12: 75-78. Proceedings, 12th International Congress of Entomology , 1 9 6 4 , L o n d o n , UK. S I T H A N A N T H A M , S., T A H H A N , O . , H A R I R I , G . , a n d R E E D , W . 1 9 8 1 . T h e i m p a c t o f winter s o w n c h i c k p e a s E L M O S A , H . 1979. Insect s p e c i e s b e l o n g i n g t o L e p i - on insect pests and their m a n a g e m e n t . P r e s e n t e d at the d o p t e r a in J o r d a n . Dirasat 6: 7-16. W o r k s h o p on Ascochyta Blight a n d Winter S o w i n g of E L M O S A , H . 1 9 8 1 . FAO/UNEP Near East Inter-Country C h i c k p e a s . I C A R DA , M a y 1 9 8 1 , A l e p p o , Syria. 12 pp. P r o g r a m for t h e D e v e l o p m e n t a n d A p p l i c a t i o n of Inte• S T A M , P.A., and S A B E K , S . 1 9 8 1 . B i o - c o n t r o l a n d t h e g r a t e d Pest C o n t r o l in C o t t o n G r o w i n g . 1 9 8 0 report. 44 pp. i m p o r t a n c e of s o m e insect pests on c o t t o n in Syria. FAO (Food and Agriculture Organization). 1981. P r o • Report for 1980 Near East Regional Programme, Inte• d u c t i o n y e a r b o o k 1 9 8 1 , vol. 34. R o m e , Italy: F A O . grated Pest Control, F A O / U N E P / 0 1 0 8 / 7 6 / 0 3 . 5 5 pp.

G E N T R Y , J . W . 1965. C r o p insects o f N o r t h e a s t A f r i c a - T A L H O U K , A.A. 1969. Insects and mites injurious to S o u t h w e s t Asia. U.S. D e p a r t m e n t of A g r i c u l t u r e H a n d • c r o p s in M i d d l e Eastern countries. H a m b u r g : Verlag Paul b o o k N o . 2 7 3 , W a s h i n g t o n D C , USA. Parey. 2 3 9 pp.

H A R I R I , G . 1972. T h e e c o n o m i c i n s e c t s o f Syria a n d W I L T S H I R E , E.P. 1957. T h e Lepidoptera of Iraq. M i n i s • n e i g h b o u r i n g c o u n t r i e s , Part 1. University of A l e p p o , try of Agriculture, B a g h d a d , Iraq. 162 pp. Syria, 4 6 5 pp. Z A H E D I , K. 1968. Lotta antiparasitaria della piante H A R I R I , G . 1 9 7 9 . Insect pests o f c h i c k p e a a n d lentils i n orteusi nell. Iran Faculty of Agriculture, University of t h e c o u n t r i e s of the Eastern M e d i t e r r a n e a n : A review. T e h e r a n Publication 102, T e h e r a n , Iran. Pages 120-123 in F o o d l e g u m e i m p r o v e m e n t a n d d e v e l • o p m e n t (eds. G.C. H a w t i n a n d G.J. C h a n c e l l o r ) . I C A R D A - I D R C p u b l i c a t i o n , A l e p p o , Syria. 2 1 6 pp.

I L E R I , M . 1960. Cukurova Pmnklarinda Zarali Yesil Kurt (Heliothis obsoleta F.) nin Yasayisi Salgin iasmasi ve onlenme earlleri uzerinde ara. Stir malar Ankara Ziraat M u c a d e l e M u d e r r a d e . A n k a r a , T u r k e y 1 6 : 6 4 . (In Turkish).

M A M E D O V A , S.R. 1978. W a y s o f i m p r o v i n g t h e m e t h o d of p r o t e c t i n g c o t t o n . R e v i e w of A p p l i e d E n t o m o l o g y Ser• ies A 6 8 : 1 1 8 0 .

M A M E D O V A , S.R., G U S E I N O V , D . G . , and I S M A I L O V , F. Y u . 1975. T h e t a c t i c s of c o n t r o l of the c o t t o n b o l l w o r m in Azerbaidzhan. Review of Applied Entomology Series A 65: 3 3 4 .

M A R T I N , H . E . 1 9 7 1 . List o f plant pests a n d d i s e a s e s i n Saudi Arabia. Near East Plant Protection Committee, F A O , C a i r o , Egypt. 55 pp.

M O R A D E S H A G I , J . , a n d P O O R M I R Z A , A . A . 1976. Laboratory studies on host preference and insecti• c i d e r e s i s t a n c e of t h e c o t t o n b o l l w o r m , Heliothis obsoleta. F. Bull. O r g . E u r o p . M e d . Prot. PI. 6: 3 1 5 - 3 2 1 .

O N G O R E N , K., K A Y A , N . , and T O R K M E N , S . 1 9 7 7 . Investigations on the morphology, bio-ecology and c o n t r o l m e t h o d s of t h e t o m a t o f r u i t w o r m (Heliothis armig-

373

Progress and Problems in Heliothis Management in Tropical Southern Africa

J.A. Gledhill*

Abstract

Heliothisarmigera in southern Africa occurs on a wide variety of wild hosts and is a damaging pest of many crops, of which cotton is the most important in terms of control costs. Although predominantly a summer pest. H. armigera is recorded as damaging on both summer and winter crops, and is of economic importance throughout the year in some part of the region. Ten years' records show that the timing of attack on any particular cotton crop is not predictable within useful limits, and the efficiency of control measures therefore depends upon field scouting to assess pest incidence and the need for insecticidal applications. The economic threshold for action to control H. armigera attack is also variable, and is affectedby climatic factors and farming practices as well as crop variety. Low-level insecticide resistance in H. armigera populations has been recorded in both Zimbabwe and South Africa in recent years, though the problem has not yet caused serious economic losses. However, with the planned intensification of agricultural production and expected extension of double-cropping irrigation schemes, the probability of the induction of resistance is steadily increasing. The general introduction of crop scouting to limit insecticide usage to essential periods, together with the development of biologically selective control measures and the improvement of pesticide application methods are suggested as priorities in the development of sound management practices for Heliothis.

*Cotton Research Institute, Gatooma, Zimbabwe.

International Crops Research Institute for the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India 375 Heliothis armigera is a pest of e c o n o m i c impor• toes and other irrigated vegetable crops during the t a n c e on a very w i d e range of c r o p s in southern winter season, f r o m May to September. On citrus it Africa, principally cotton, but including various is r e c o r d e d (Pearson 1958) from the e n d of August beans, castor, carnations, chickpea, citrus, coffee to O c t o b e r a n d it c a n c a u s e d a m a g e to irrigated (young leaves), groundnut, maize, peas, sorghum, winter wheat during the soft d o u g h stage over a stocks, sunflower, sunnhemp, tobacco, tomato, similar period. a n d w h e a t (PPRI 1980). In the Republic of South Heliothis armigera d a m a g e to Virginia t o b a c c o Africa additional c r o p hosts r e c o r d e d are apples, ( T o b a c c o R e s e a r c h Board 1980) is most likely to boysenberries, cherries, cruciferae, cucurbits, o c c u r b e t w e e n O c t o b e r and D e c e m b e r , within 8 lucerne, lupines, ornamentals, peaches, pears, w e e k s of transplanting. On cotton it has bee n plums, quinces, vines, and youngberries (Bot et al. recorded from October to June, virtually throughout 1980). H. armigera also o c c u r s on a w i d e range of the legal cotton period, a n d also on out-of-season wild hosts, including s o m e flowering trees and experimental crops at Gatooma and in the Zambesi shrubs s u c h as Cassia spp. An H. armigera larva Valley b e t w e e n M a y a n d September. Although the w a s r e c o v e r e d f r o m a wild winter-flowering Cassia pupal d i a p a u s e (Pearson 1958) may facilitate pop• at Gatooma during bush surveys carried out in ulation carryover under the normally dry winter 1970, but there are no other records of Heliothis on conditions, it seems probable that the increasing wild trees. Laboratory feeding tests in September at winter irrigation is providing opportunities for a c o n • G a t o o m a h a v e indicated that Brachystegia spici- tinuous progression of nondiapause generations to formis, Schotia brachypetala, a n d Erythrina abys- persist all year round. sinica flowering heads are readily taken by all T h e incidence of d a m a g i n g levels of H. armigera stages of H. armigera larvae. Larval development on cotton, as indeed on other crops, is highly varia• was almost identical for Brachystegia, Schotia, and ble. Table 1 summarizes ten years of cotton pest the standard b e a n a n d maize meal Heliothis diet, r e s e a r c h records of the periods during w h i c h pesti• but w a s slower for larvae feeding on Erythrina. c i d e spray control of Heliothis was required In c o n s i d e r i n g the problems a n d possibilities (Gatooma Research Station 1969, 1970, 1971, c o n n e c t e d with Heliothis m a n a g e m e n t in this 1972, 1973; Brettell et al. 1974-1981) at (a) region, it must be recognized that besides the wide Gatooma Research Institute on raingrown cotton range of potential hosts, there is also a w i d e range g e r m i n a t e d b e t w e e n 5 N o v e m b e r a n d 10 of climatic and environmental conditions under D e c e m b e r a n d (b) Chiredzi R e s e a r c h Station on w h i c h the hosts may occur. T h e r e is also a wide irrigated cotton germinated about the first week of range of farming practices and levels of agricultural N o v e m b e r . inputs applied in different cropping systems, having It must be emphasized that these examples differing i m p a c t s on the stability or instability of apply to w e l l - m a n a g e d trial crops on research sta• Heliothis populations through the seasons. tions. M u c h greater variations o c c u r under farm The cost of Heliothis control is greater for cotton conditions ranging from s o m e very long-season t h a n for any other c r o p in the region; this paper will irrigated crops to s o m e very short-season rainfed therefore deal basically with the problems of H. c r o p s in the w a r m e r a n d drier areas. armigera in cotton a n d s o m e recent d e v e l o p m e n t s At G a t o o m a the incidence of H. armigera has in its control a n d m a n a g e m e n t , while introducing also b e e n monitored by a Robinson light trap for the other crops w h e r e appropriate. past 10 years, and graphical comparisons of light- trap records of H. armigera m o t h c a t c h e s a n d c o n • temporaneous weekly records of egg counts from The Seasonal Incidence field trials are s h o w n in Figure 1. This figure gives: of Heliothis 1 T h e weekly totals of H. armigera moths caught Heliothis armigera has been r e c o r d e d attacking by the light trap during e a c h cotton cropping different c r o p s at all s e a s o n s of t h e year in Z i m • s e a s o n from 1971 -72 to 1 9 8 0 - 8 1 . T h e n u m b e r s babwe, but is predominantly a pest during the are g r a p h e d on a logarithmic scale against s u m m e r rainy season. In the winter months it is w e e k s a n d for the week of full m o o n , moth m o r e prevalent in t h e w a r m e r environments, with n u m b e r s are c o r r e c t e d upwards, w h e r e n e c e s • monthly m e a n temperatures about 15°C, than in sary, to the geometric m e a n b e t w e e n the the cooler uplands. It c a n be d a m a g i n g on t o m a - p r e c e d i n g a n d s u c c e e d i n g w e e k l y m o t h

3 7 6 Table 1. Duration of damaging Heliothis attack in cott on trials 1070/71-1980/81.

Gatooma (1157m) Chiredzi (430m) Jan Feb Mar Apr May N o v D e c J a n F e b M a r A p r

Earliest and latest dates of a t t a c k o v e r 1 0 y e a r s 1 8 w e e k s 1 7 w e e k s x------x x------x

Longest seasonal attack 1 1 . 5 w e e k s 1 1 w e e k s x ------x x------x

Shortest seasonal attack 3 w e e k s 3 w e e k s x- - -x x- - -x Common attack period over 10 years 2 w e e k s 3 w e e k s x- - x x - - - x

Common attack period 4 years in 5 6 w e e k s 6 w e e k s x- - - -x x - - - -x

catches. Light-trap moth catches are almost inspection and scouting for pest incidence if unne• always reduced during full moon. cessary insecticide applications are to be avoided. 2The mean weekly H. armigera egg counts per 100 plants, recorded from the weekly scouting of 420 to 600 randomly selected plants in the General Considerations for Heliothis insecticides trial at Gatooma, which is Heliothis Control conducted annually. 3.The weekly rainfall total (mm) recorded at the For cotton, scouting procedures are needed to Cotton Research Institute. assess the incidence of at least five key pests, 4.The recommended timing of insecticide spray• including Heliothis. For this reason sequential sam• ing for H. armigera control, based upon an pling has not been developed for farm use, since

action threshold (A/TE ) of 50 eggs per 100 the full sample size is virtually always required. plants (12/24 plants), or a cumulative count Standard practice is to scout weekly 24 plants

exceeding the A/TE over 2 or 3 consecutive (Gledhill et al. 1972) per field of up to 20 ha on a unsprayed weeks, or a rising count the projec• stratified sampling pattern. Where pest levels are

tion of which would exceed A / T E by the next close to the prescribed action threshold, an addi• week. Late-season sprays due according to the tional check count is recommended to verify the A / T E after the cotton had reached maturity are results; other factors related to yield potential may marked as cancelled. also be used in deciding whether or not to spray a broad-spectrum insecticide. During the main cotton flowering and fruit- Chemical pest-control trials in Zimbabwe are formation period, mid-February to mid-April, the aimed at establishing minimal effective field dos• correlation between moth catches and Heliothis age rates for Heliothis pesticides, assessed on the egg counts is often quite good, but discrepancies basis of 7-day intervals between spray applica• between the two may be large at the start of many tions, when egg incidence is above the action seasons and also during the course of some sea• threshold. sons such as 1972-73, which was a drought year: Minimal effective dosage rates on full-grown cot• 1975-76, when cotton germination was very late; ton for recommended Heliothis insecticides and 1980-81, which was unusually wet. assessed at two research station sites in Zim• In view of the unpredictability of the time of Helio• babwe over the past 12 years are given in Table 2. this attack on cotton crops in different places in the Carbaryl 85% WP at 1000 g ai and endosulfan at same season, or the same place in different sea• 300 g ai with 10% to 25% molasses as diluent are sons, or on adjoining crops of different ages in the also recommended for Heliothis control but are not same season, the efficient timing of Heliothis c o n • quite as active as the other chemicals listed. trol measures is completely dependent upon crop Concurrent research is conducted on scouting

377 Weekly moth trap catch totals Weekly egg counts/100 plants

Trap catch adjusted for full moon Weekly rainfall (mm)

Spray 500 200 Cancelled spray 100 1971-72 50 Egg action threshold A/TE 150 20 10 100 7 5 3 50 2 s s s s s s s s s 5 12 19 26 2 9 16 23 30 6 13 20 27 6 13 20 27 3 10 17 24 1 8 15 22 29 December January February March April May

500 1972-73 200 100

50 Egg action threshold A/TE 20 150 10 100 5 3 50 2 S S S

5 12 19 26 2 9 16 23 30 6 13 20 27 6 13 20 27 3 10 17 24 1 8 15 22 29 December January February March April May

500 1975-76 200 100 50 Egg action threshold A/TE 20 150 100 10 50 2 S S S S S S

5 12 19 26 2 9 16 23 30 6 13 20 27 6 13 20 27 3 10 17 24 1 8 15 22 29 December January February March April May

1980-81 500 200 100 50 A/TE A/TE 150 20 10 100

I NR 50 3 2 S S S S S S

5 12 19 26 2 9 16 23 30 . 6 13 20 27. 6 13 20 27 3 10 17 24 . 1 8 15 22 29 December January February March April May

Figure 1. Light-trap and insecticide trials for Heliothis armigera control, field records, Gatooma Research Station, Zimbabwe: 1971-72, a normal year; 1972-73, a drought year; 1975-76, cotton germination unusually late; 1980-81, an unusually wet year.

3 7 8 five a n d flexible m a n a g e m e n t with the i m p l e m e n t a • T a b l e 2 . R e l a t i v e f i e l d activity o f r e c o m m e n d e d tion of weekly or twice-weekly c r o p scouting a n d Insecticides against Heliothis armigera In Zimbabwe. cross c h e c k i n g , the season c a n be divided into four periods, during which different criteria for timing of R a t e o f c h e m i c a l spray applications against Heliothis are Insecticide Formulation a p p l i c a t i o n / h a appropriate.

DDT (limited 1. Early growth period: prior to the formation of recommenda- potentially productive squares (time of first t i o n ) 7 5 % WP 1 0 0 0 g a i E n d o s u l f a n 3 5 % M O 5 0 0 g a i effective squares) ( H e a m a n d R o o m 1979), Cypermethrin 2 0 % E C 3 0 g a i spray decision is m a d e on weekly larval Deltamethrin 2 . 5 % E C 6 . 2 5 g a i counts, with an action threshold of up to 18 Fenvalerate 2 0 % E C 4 0 g a i larvae on 24 plants. T h e aim is to limit the use of b r o a d - s p e c t r u m pesticides during this period, a n d biological control agents or selective c h e m i c a l insecticides woul d be methods and the practical determination of spray most useful here. timing, using action thresholds applicable in the 2. Early squaring and fruiting period: from first existing w i d e range of farming conditions. productive square formation to about the s e c o n d week (depending on climate) of pro• ductive flower formation. Spray decision is Action Thresholds and Spray m a d e on weekly egg a n d larval counts, with Timing for Chemical Control an action threshold of 12 eggs (or 6 larvae) of Heliothis on Cotton on 24 plants. 3. Main fruiting period: from period 2 until 2 T h e o p t i m u m timing of insecticide applications is w e e k s after estimated date of last productive subject to a range of factors, s o m e of w h i c h , like flower. This should not be longer than about 8 weather, c a n alter crop potential within wide limits, weeks. Spraying decision is m a d e on weekly a n d are b e y o n d major remedy, but must be taken action threshold of: (a) counts of 8 eggs per into account. Others, s u c h as levels of pest inci• 24 plants, or (b) cumulative c o u n t s of 8 eggs dence, p r o d u c e fairly predictable short-term per 24 plants from 2 or 3 c o n s e c u t i v e w e e k s effects that are a m e n a b l e to corrective action. without spray applications, or (c) rising e g g Practical r e c o m m e n d a t i o n s on spray timing ( G l e d - counts, the projection of w h i c h woul d e x c e e d hill 1977) that will avoid the use of potentially 8 per 24 plants by the next week. wasteful calendar spraying have to be tailored to 4. Crop maturing period: spray decision is meet the different users' resources a n d require• m a d e on 10- to 14-day action threshold of 12 ments. This calls for a gradation of r e c o m m e n d a • eggs per 24 plants until all productive bolls t i o n s f r o m t h e m o s t s i m p l e t o t h e m o s t have r e a c h e d the fibrous stage; thereafter sophisticated, suited to the different farming practi• Heliothis control is not required c e s a n d conditions. Given the ability to recognize a n d count Heliothis W h e r e c r o p scouting is c o n d u c t e d twice weekly, eggs, the simplest set of r e c o m m e n d a t i o n s relate spray action on e g g thresholds c a n be delayed by 3 to late-germinated rainfed cotton with a strictly or 4 days if pest control, as indicated by low larval limited growing season. In s u c h c a s e s , any Helio• counts, retains effectiveness for more than a week. this attack a b o v e a given action threshold b a s e d on This allows the spray interval to be extended to 10 e g g c o u n t s (normally 12 eggs per 24 plants) would days or 2 w e e k s w h e r e justified by insecticidal justify a spray application. A simple yes or no spray persistence or any other c a u s e of high pest decision is required weekly. mortality. At the other e n d of the s c a l e is t h e detailed M a n y larger f a r m s a n d estates in Z i m b a b w e pay p r o c e d u r e n e e d e d for deciding o p t i m u m pest- a hectarage fee to participate in an external c h e c k m a n a g e m e n t practices in cotton c r o p s with a long scouting s c h e m e , w h i c h operates to supplement d e p e n d a b l e growing s e a s o n w h e n water a n d their farm scouts. T h e c h e c k scouting s c h e m e is temperature are not normally limiting. Under effec- organized by the C o m m e r c i a l Cotton G r o w e r s

379 Association and provides for weekly checks as well resulted in the heavy use of pesticide mixtures at all as monthly, or more frequent, group discussions stages of cotton crop development. Cotton plant• with extension specialists. ings had been made from early October to mid- December, and the resultant spraying program on successive fields continued from mid-October to Heliothis Resistance May or June. to Insecticides Under the revised spraying program, minimal insecticide sprays were applied against Heliothis In Zimbabwe, despite fairly intensive insecticidal (spray threshold of 18 larvae per 24 plants or treatments against Heliothis on about 100 000 ha of 25000 larvae/ha) during the period from germination cotton annually, in rather widely dispersed areas, up to 27 December (period P1, Fig. 2). Thereafter, there has only been one established instance (in during the main crop-formation period through 1978) over the past 10 years of insecticide resist• crop maturity, (period P2, Fig. 2) Heliothis control a n c e in a Heliothis population. Although it was not sprays were applied at the standard spray thre• possible to carry out a full-scale comparative shold of 12 eggs or 6 larvae per 24 plants, and a bioassay between the field strain from Chisum- synthetic pyrethroid was introduced into the spray banje Estate and the laboratory standard culture, program for the first time. the limited tests that were completed with insecti• In the 1978-79 season, cotton germination on cide concentrations close to the normal LC50s the estate extended over 10 weeks. For the pur• showed tolerance levels for both endosulfan and pose of analysis, scouting records from all fields DDT that were from 1.6 to over 2.5 times higher in (total area of 2295 ha) were assembled into 10 the field strain (Madende and Brettell 1978). groups. Mean egg and larval counts from cotton In South Africa, tolerance of Heliothis armigera to fields with the same week of germination were endosulfan (3 times) and parathion (5 times) was computed separately for period P1 and period P2. reported by Whitlock in 1973. More recently, Bas- These are shown in Figure 2, together with the main son (1980) investigated reports of unsatisfactory yields for each group. control of H. armigera by endosulfan in some The marked differences in the intensity of Helio• cotton-producing areas in the northern and eastern this attack on cotton fields of different ages is note• Transvaal. On bioassay, he found resistance fac• worthy, and emphasizes the importance of field tors of 2.1 and 0.7 over the laboratory standard in scouting for the determination of pest threshold larvae from Komatipoort in the 1976-77 and 1977- levels rather than dependence upon nonspecific 78 seasons. Subsequently, endosulfan had been assessments of pest incidence. replaced by synthetic pyrethroids for Heliothis c o n • It appears unlikely that the high Heliothis larval trol in these areas, with satisfactory results, but populations during period 1 on the earlier planted Basson advised continued monitoring to check for fields had any appreciable adverse effects upon Heliothis resistance to the insecticide currently in yield. The highest single yield of the season was use. from a field that germinated in the week ending 21 In the case of resistance at Chisumbanje in October; and this yielded 3716 kg/ha seed cotton Southeastern Zimbabwe, the estate management despite mean larval counts of more than 45 per 100 decided to adopt a new pest-control program in plants over 8 weeks in period P1. Factors other than 1978-79, following research recommendations early Heliothis attack were obviously important in (Gledhill 1980) aimed at reducing the risk of build• determining yield. ing up insecticide resistance in Heliothis. C h i s u m • The number of Heliothis control sprays applied to banje is a fully irrigated estate of over 2000 ha each group of fields in periods P1 and P2 are shown growing summer cotton and winter wheat. Heliothis in Table 3, together with the number of carbaryl populations persist throughout the year, and heavy sprays applied for Diparopsis castanea (red boll- attack usually develops on seedling cotton in worm) control. These carbaryl sprays would also October and November during which period there have provided some degree of control of Heliothis. are virtually no other green plants, either cultivated Heliothis larvae were collected from the Chisum• or wild, available to egg-laying moths. For a numbe r banje Estate in February 1979 and used to initiate a of years previously, the pest spraying program had separate laboratory culture at the Cotton Research been based upon the simple premise that high Institute in Gatooma. This was subsequently com• input equals high production; this approach pared with the standard Gatooma laboratory strain

3 8 0 8 0 3 2 0 0 7 5 3 0 0 0

7 0 2 8 0 0 6 5 2 6 0 0 6 0 2 4 0 0 5 5 2 2 0 0 5 0 4 5 4 0 3 5 30 2 5 20 1 5 10

0 P1 P2 P1 P2 P1 P2 P1 P2 P1 P2 P1 P2 P1 P2 P1 P2 P1 P2 P1 P2 N o . of w e e k l y c o u n t s 8 19 8 19 8 20 8 18 7 19 6 19 7 19 4 22 4 21 2 21 W e e k o f g e r m i n a t i o n 7 O c t 1 4 O c t 2 1 O c t 2 8 O c t 4 N o v 1 1 N o v 1 8 N o v 2 6 N o v 3 D e c 1 0 D e c

Figure 2. Heliothis armigera egg and larval counts from weekly scouting records, Chisumbanje Estate, Southeastern Zimbabwe, 1978-79 season. P1 = period 1, before 28 December; P2 = Period 2, after 28 December; E1 and L1 = egg and larval counts in Period 1; E2 and L2 = egg and larval counts in period 2; Y = yield of seed cotton.

Table 3. Mean number of bollworm sprays applied to cotton on Chisumbanje Estate, southeastern Zimbabwe.

P e r i o d 1 P e r i o d 2 Week of T o t a l (Germination to 27 Dec) (27 D e c to G r o u p germination area m a t u r i t y ) Y i e l d N o . 1 9 7 8 (ha) Diparopsis Heliothis Heliothis ( k g / h a )

1 7 . 1 0 6 4 2.5 1.5 8.0 2619 2 1 4 . 1 0 32 2 . 3 1.6 8 . 1 2 7 9 6 3 2 1 . 1 0 317 1.5 1.9 6 . 8 2 5 6 4 4 2 8 . 1 0 2 8 5 1.1 1.4 7.0 2 6 6 1 5 4 . 1 1 321 1.0 0 . 9 7.3 2338 6 1 1 . 1 1 326 0 . 4 0.8 7.6 2 6 0 9 7 1 8 . 1 1 90 0 0 . 5 8 . 5 3 0 5 1 8 2 6 . 1 1 149 0 0 . 4 9.2 3 1 2 2 9 3 . 1 2 6 0 4 0 0 . 3 8 . 3 2757 1 0 1 0 . 1 2 106 0 0 6.8 2610

381 for susceptibility to endosulfan. Replicated bioas- until March-April, but if planted a month or more says testing mortality rates of second-instar larvae before the cotton crop, it has been found to be exposed to cotton leaf discs treated with a series of much more attractive in its vegetative phase than is concentrations of endosulfan gave almost identical preflowering cotton. Under special conditions of LC50s for both strains (Madende and Brettell exceptionally early H. armigera attack upon young 1979). cotton (as at Chisumbanje, see Figure 2) this might very well reduce the attack on cotton to nondamag- ing levels. In addition, it appears that vegetative Biological Control of dolichos bean is not suitable for the complete Heliothis armigera development of H. armigera larvae and may there• fore act as a true trap crop in its vegetative phase.

Investigations into numerous aspects of biological control of the cotton bollworm by predators, paras• Reducing the Risk of ites, pathogens, trap crops, and crop breeding were Heliothis Resistance instituted in southern Africa by the Empire Cotton Growing Corporation Research Stations at Barber- Current registrations and recommendations for ton and Gatooma, starting in the late 1920s. After insecticides used against H. armigera in Zimbabwe the introduction of the broad-spectrum chlorinated take account of the desirability of limiting the inten• hydrocarbons, organophosphates, and carbam• sity of insecticide usage to reduce the chances of ates in the 1950s, the relative amount of research selecting for resistance. The need to formulate a applied to biological control diminished, but the definite policy in this regard was sharpened by the field has still continued to receive attention, eve n advent of the synthetic pyrethroids, the properties from research stations basically concerned with of which increased the likelihood of indiscriminate cotton production research. and thoughtless prophylactic insecticide applica• McKinley (1971) in Rhodesia and Roome tion. (1975a, 1975b) in Botswana investigated the use of Thus, pyrethroids are not registered for use in nuclear polyhedrosis virus and Bacillus thuringien- winter (irrigated) crops or on summer crops for sis preparations against H. armigera in cotton or which economically effective alternatives are sorghum. Roome found that the use of a local virus readily available. Recommendations are aimed at for Heliothis control on sorghum offered definite limiting the period of exposure to pesticides of any promise. Later trials with pathogens on cotton in given pest species, and at discouraging blanket Zimbabwe have confirmed McKinley's findings and spray usage. have given disappointing results except in cases Pyrethroids are registered only for cutworm con• w h e r e the B. thuringiensis preparation Dipel was trol on tobacco, involving one spray at transplant• used with chlordimeform, (Brettell et al. 1974-1979 ) ing or soon afterwards. Single applications only are but its field effectiveness was inconsistent. recommended on some other summer crops for Brettell (1979) in Zimbabwe, investigating the the control of Heliothis. tolerance to insecticide of some larval Chrysopi- for cotton, recommended practices in Zimbabwe dae predatory upon H. armigera, has found that a include: common species in cotton fields, Chrysopa boninensis, shows remarkably low susceptibility to 1. Use of selective aphicides where necessary m a n y Heliothis insecticides. for early aphid attack, thus permitting natural Some work has also been done on the incidence predator and parasite buildup. a n d use of Trichogrammatoidea sp egg parasites 2. Caution in the early use of broad-spectrum for Heliothis control in cotton. The natural inci• insecticides. dence of the parasites has proved to be very spo• 3. Use of 'conventional" endosulfan, carbaryl, radic, but apparently unaffected by insecticide or (in some cases) DDT sprays for bollworm spraying programs in the cotton fields sampled. control, if needed, until the end of January in Another biological control aid under investiga• most cotton-growing areas (late December tion in Zimbabwe is the use of dolichos bean (Peat in the warmer irrigated areas). and Prentice 1938) as a diversionary trap crop 4. Limitation in the subsequent use of synthetic against H. armigera attack on preflowering cotton pyrethroids on cotton to a period of not more (Gledhill 1980a, 1980b). Dolichos does not flower than 9 weeks in any one season.

382 5. The use of minimal dosage rates of all insec• providing for more frequent application intervals ticides, applied only when economically only if required by actual pest-control require• necessary. ments.

The fact that in this region large populations of Heliothis on wild hosts and on many summer crops, Acknowledgments such as maize, sorghum, and sunflower, do not receive any insecticidal spray treatments provides I wish to record my appreciation of assistance a large buffer population that should be fully sus• received from Dr. J.H. Brettell, who provided the ceptible to insecticides, and should be capable of Gatooma light-trap records on Heliothis m o t h diluting pockets of incipient resistance, provided catches that have been used in this paper, and adequate mobility and population mixing occurs. gave ready help with the extraction of other station This is currently presumed to be the case in most records and in reading and commenting upon the areas, although it is not factually established. Ho w • manuscript. Authority from the Director, Depart• ever, with the prospect of increasingly intensive ment Research and Specialist Services, to present crop production, this apparently favorable situation this paper is also gratefully acknowledged. cannot be expected to continue indefinitely. It is suggested that in regard to the short- and medium-term development of Heliothis m a n a g e • ment in this area, priority should be given to the References following aspects:

BASSON, N.C.J. 1981. A survey of the possible devel• 1. Establishing the use of practical action thre• opment of resistance to endosulfan by the American b o l l - sholds for Heliothis insecticide applications w o r m , H. armigera on cotton. In Proceedings, Union that can be understood and applied by all the Carbide Workshop on Cotton Pest Control, March 1980 , farmers concerned. Acceptable usage of all Nelspruit, S. Africa. In press. insecticides should eventually become con• BOT, J., VERMEULEN, J.E., and HOLLINGS, N. ditional upon prior crop inspection and 1980. A guide to the use of pesticides and fungicides in scouting. the Republic of South Africa. Department of Agricult u r a l 2. Developing biologically selective methods for Technical Services, Pretoria, South Africa. Heliothis control. Such methods would not have to possess particularly high levels of BRETTELL, J.H., BEMONT, M.J.L., and DURURU, PC. 1974-1979. Biological control trials. I n C o t t o n efficacy in order to be of value. The imme• Research Institute Annual Reports: Pages 102-105 in diate need is for treatments that can be used 1974/75; pages 167-170 in 1975/76; pages 158-160 in safely when larval thresholds of economic 1977/78; pages 158-161 in 1978/79, annual reports, damage on crops are relatively high, with the Gatooma, Zimbabwe. aim of containing Heliothis populations with• BRETTELL, J.H., AND ASSOCIATES. 1974- out disrupting natural control processes. 1 9 8 1 . B o l l w o r m insecticides trials. In Cotton Research 3. Reducing spray application costs and simpli• Institute Annual Reports: Pages 87-90 in 1973/74; pages fying methods available for effective pesti• 1 2 2 - 1 2 6 in 1974/75; pages 141-150 in 1975/76; pages cide application. This would increase the 1 8 0 - 1 8 4 in 1976/77; pages 145-149 in 1977/78; and relative cost of chemicals against the costs pages 147-151 i n 1978/79 annual reports. 1979/80 and of application and would diminish the attrac• 1980/81 annual reports in press. Gatooma, Zimbabwe. tiveness of high dosage rates intended to BRETTELL, J.H. 1979. Green lacewings (Neuroptera: provide longer persistence and fewer spray Chrysopidae) of cotton fields in central Rhodesia. 1. B i o l - applications. Such practices often result in o g y of Chrysopa boninensis Okamoto and toxicity of cer- heavy overdosing and unnecessary pesti• tain insecticides to the larva. Rhodesian Journal of cide presence, causing ecological damage. Agricultural Research 17: 141-150.

GATOOMA RESEARCH STATION. 1969, 1972, and The simplification of application methods would 1973. Bollworm insecticide trials. Pages 27-35 in make it easier to promote the use of biological 1 9 6 8 / 6 9 ; p a g e s 5 9 - 6 1 in 1971 /72; and pages 68-71 in insecticides and the use of lower chemical insecti• 1972/73 Annual reports, Gatooma Research Station, cide dosage rates, giving shorter persistence and Z i m b a b w e .

3 8 3 GLEDHILL, J.A., ET AL. 1972. Bollworm scouting trials, TOBACCO RESEARCH BOARD. 1980. T o b a c c o pages 84-85 i n G a t o o m a R e s e a r c h Station a n n u a l report Research Board Recommendations, 1980. TRB, Kut- a n d p a g e s 1 3 6 - 1 3 9 i n 1 9 7 4 / 7 5 C o t t o n R e s e a r c h Institute saga, Zimbabwe. annual report, Gatooma, Rhodesia. WHITLOCK, V.H. 1973. Studies on insecticidal resist• GLEDHILL, J.A. 1977. C r o p l o s s e s i n c o t t o n c a u s e d b y a n c e in t h e b o l l w o r m H. armigera. P h y t o p h y l a c t i c a 5: Heliothis a n d Diparopsis bollworm. Rhodesia Agricultural 7 1 - 7 4 . J o u r n a l 73: 1 3 5 - 1 3 8 .

GLEDHILL, J.A. 1981a. Measures taken against pesti• c i d e resistant Heliothis p o p u l a t i o n in t h e R h o d e s i a n low- veld. In P r o c e e d i n g s , U n i o n C a r b i d e W o r k s h o p on C o t t o n Pest Control, March 1980, Nelspruit, S. Africa. In press.

GLEDHILL, J.A. 1981b. D o l i c h o s t r a p c r o p p i n g trial for Heliothis. In C o t t o n R e s e a r c h Institute a n n u a l report 1979/80, Gatooma, Zimbabwe.

HEARN, A.B., and ROOM, P.M. 1979. Analysis of crop development for cotton pest management. Protection Ecology 1:265-277.

McKINLEY, D.J. 1971. Nuclear polyhedrosis virus of the c o t t o n b o l l w o r m i n C e n t r a l A f r i c a . C o t t o n G r o w e r s R e v i e w 48: 297-303.

MADENDE, M., and BRETTELL, J.H. 1978. Laboratory screening of insecticides. Pages 178-179 in C o t t o n Research Institute annual report 1977/78, Gatooma, R h o d e s i a .

MADENDE, M., and BRETTELL, J.H. 1979. Laboratory screening of insecticides. Pages 172-173 in C o t t o n Research Institute annual report 1978/79, Gatooma, Z i m b a b w e .

PPRI (Plant Protection Research Institute). 1970, 1 9 7 1 . Bollworm insecticide trials. Pages 30-37 in 1 9 6 9 / 7 0 A n n u a l report a n d p a g e s 2 1 - 2 5 i n 1 9 7 0 / 7 1 Annual report. PPRI, Rhodesia.

PPRI (Plant Protection Research Institute). 1 9 8 1 . Departmental records 1980/81. Plant Protection R e s e a r c h Institute a n d C o t t o n R e s e a r c h Institute, D e p a r t • ment of Research and Specialist Services, Zimbabwe.

PEARSON, E.C. 1958. T h e insect p e s t s o f c o t t o n i n tropical Africa. London, UK: Commonwealth Institute of Entomology.

PEAT, J.E., and PRENTICE, A.N. 1938. C o t t o n Station progress report, Gatooma, Southern Rhodesia. Pages 71 - 72 in E m p i r e C o t t o n G r o w i n g C o r p o r a t i o n Report, Gatooma, Rhodesia.

ROOME, R.E. 1975a. Fixed trials w i t h a n u c l e a r polyhedrosis virus and Bacillus thuringiensis against lar• v a e of Heliothis armigera on s o r g h u m a n d c o t t o n in B o t s • wana. Bulletin of Entomological Research 65: 507-514.

ROOME, R.E. 1975b. Activity of adult Heliothis armigera w i t h r e f e r e n c e t o t h e f l o w e r i n g o f s o r g h u m a n d m a i z e i n Botswana. Bulletin of Entomological Research 65: 523- 5 3 0 .

3 8 4 Research on Heliothis at ICRISAT

V.S. Bhatnagar, S.S. Lateef, S. Sithanantham, C.S. Pawar, and W. Reed

Abstract

ThelnternationalCropsResearchlnstitute tor the Semi-Arid Tropics(ICRISAT) has a mandate to improve the production of sorghum, pearl millet, groundnut, pigeonpea, and chickpea. All of these crops are susceptible to H e l i o t h i s spp. and survey data show that both pigeonpea and chickpea suffer crop loss to these pests in almost all the areas of the world where they are grown. The recent progress in research on various aspects of the ecology and management of Heliothis armigera at the ICRISAT Center in India is reviewed: population studies using light and pheromone traps; pesticide use; natural control elements, including parasites, predators, and diseases; cultural and cropping practices, including mono- and inter-crop comparisons; and host-plant resistance screening and breeding, including mechanisms of resistance. The potential tor the development of integrated pest management that will be of practical benefit in farmers' fields is also discussed.

The International Crops Research Institute for the been recorded on more than 100 other plant spe• Semi-Arid Tropics (ICRISAT) has the mandate to cies in this area. This pest causes greatest losses improve the production of five crops: sorghum, on pigeonpea and chickpea, so our major efforts in pearl millet, groundnut, pigeonpea, and chickpea. Heliothis research have been concentrated upon The small farmers with very limited resources, who these two crops. form the great majority of the farmers in the semi- Although chickpea and pigeonpea are not very arid tropics, are our special target. Our clients are well known in the world's food markets, they are of the agricultural research and development workers enormous importance in some parts of the semi- of the national and regional programs, to whom we arid tropics, particularly In the Indian subcontinent, supply information and materials, particularly new where 80% of the world's chickpea and 90% of the germplasm, which can be locally adapted and world's pigeonpea crops are grown. They are the developed for the benefit of the farmers. two major pulse crops of the region, providing a All five of ICRISAT's mandate crops are suscept• valuable protein supplement to the diets of the ible to Heliothis spp. At ICRISAT Center, Heliothis predominantly vegetarian human population. armigera damages all of these crops and has also On pigeonpea, as on most other hosts, Heliothis spp larvae are mainly pests of the flowering and

*International Crops Research Institute for the Semi-Arid Tropics fruiting stages of the crop. On chickpea, however, (ICRISAT), Patancheru, Andhra Pradesh, India. the plants are attractive to egg laying by Heliothis

International Crops Research Institute tor the Semi-Arid Tropics. 1982. Proceedings of the International Workshop on Heliothis Management, 15-20 November 1981, Patancheru, A.P., India 3 8 5 spp from the seedling stage and substantial dam• in the north where the crop matures after the winter, age can be caused throughout the vegetative and at a time when these pests have had insufficient podding stages of this crop. time to build up to large populations. In the northwest, however, there is substantial cropping of early-maturing pigeonpeas, which are harvested before the winter, and these are often severely Surveys of Pest Damage in d a m a g e d by Heliothis. The second most damaging Chickpea and Pigeonpea pest of pigeonpea in India is the podfly, Melana- gromyza obtusa, which tends to be of most impor• tance in the central and northern areas in the Crop Damage in India late-maturing crops. In southern India, more than one-third of the As there were no wide-scale survey data of losses pods on average, but much more in some areas caused by pests in farmers' crops of pigeonpea and years, are damaged by H. armigera. Further, and chickpea, ICRISAT embarked upon one, start• we are aware that H. armigera not only d a m a g e s ing in 1975, in cooperation with national entomolo• the large pods, which are retained on the plant and gists. This survey has been particularly active in so can be counted in our survey samples, but it also India, where we have visited and assessed the pest destroys large numbers of buds, flowers, and damage in 1297 fields of pigeonpea and 645 fields young pods, which are shed, so our survey data of chickpea in the major producing areas of the can grossly underestimate the damage caused by country. this pest. Pigeonpea suffers damage from a large complex Chickpea has a relatively small number of insect of insect pests including several species of lepi- pests of which Heliothis spp are dominant in all the dopteran larvae, which feed upon the flowers and major production areas of the world. In India we pods, but H. armigera is by far the most important of have collected pod samples from more than 600 these. Our surveys are timed to collect samples of farmers' fields and found an average of 7.5% of pods from the crop at the maturity stage. These pods d a m a g e d by H. armigera. Here again, this samples are brought to our laboratory, where a grossly underestimates the actual losses caused, skilled team assesses the percentage of pods that for there can be severe vegetative and flower feed• have been damaged by the various pest groups. ing, particularly in central and southern India. This The data that were recorded from these surveys crop grows through the winter, and in most years in across India are shown in Table 1. northern India it is harvested before H. armigera It can be seen that damage caused by lepidopte- populations build up to damaging levels. In some ran larvae (mostly H. armigera) tends to d e c r e a s e years and areas, however, the crop is hit by mas-

Table 1. Pigeonpea pod damage by insects in samples from farmer' fields In India, 1975-1981.

N o r t h w e s t N o r t h C e n t r a l South z o n e z o n e z o n e z o n e E a r l y - L a t e - M i d - a n d E a r l y - a n d m a t u r i n g m a t u r i n g l a t e m i d m a t u r i n g m a t u r i n g

F i e l d s s a m p l e d ( n o . ) 49 3 5 9 446 4 4 3

P o d s d a m a g e d b y l e p i d o p t e r a n b o r e r s (%) 2 9 . 7 1 3 . 2 2 4 . 3 3 6 . 4

P o d s d a m a g e d by p o d f l y (%) 1 4 . 5 2 0 . 8 2 2 . 3 11.1

T o t a l p o d s d a m a g e d b y i n s e c t p e s t s (%) 4 4 . 0 3 3 . 8 4 8 . 0 4 9 . 9 sive populations of this pest, perhaps as a result of will eventually understand the major factors migration, and the crop can be completely influencing these populations and so be able to destroyed. forecast the incidence of damaging populations in any area.

Crop Damage in Other Countries Egg and Larvae Counts

In line with our international mandate, we also take The polyphagous habit of Heliothis spp compli• every opportunity to collect data on the pests and cates the estimation of populations by direct the losses that they cause in other countries where counts of eggs and larvae, for there are so many these crops are of importance. We collect such hosts. At ICRISAT Center our pest surveillance data by visits and through correspondence with team counts H. armigera eggs and larvae on sam• local entomologists. In all areas of the world where ple areas of all our crops on the pesticide-treated pigeonpea is of importance, Heliothis spp are the areas. The summarized data from these counts are dominant pests. In eastern Africa, H. armigera illustrated in Figure 1. Here it can be seen that our severely damages the crop. In the Caribbean, both crops provide food for Heliothis from late July until H. zea a n d H. virescens are common pests of April, when a closed season of 2 months, during pigeonpea pods. In our cooperative studies with which no crops may be grown, begins. We adopted ICARDA on the pests of chickpea in Syria, we have this closed season in an attempt to reduce our pest found that H. armigera a n d H. viriplaca (syn H. problems, which had become particularly severe, dipsacea) cause major damage, in addition to the partly because there was continuous availability of leaf miner, Liriomyza cicerina, which can cause crops at all stages of growth throughout the year. In crop loss in most of the Mediterranean and west the past 2 years we have reduced H. armigera Asian chickpea-producing countries. In Mexico populations within the ICRISAT boundaries virtu- and other American countries, both H. zea a n d H. ally to nil during this closed season. Outside our virescens are known to cause substantial crop loss boundaries however, H. armigera can be found in chickpea. through the hot and dry April to June period in reduced but substantial populations on a variety of weed hosts and on irrigated tomatoes. Monitoring and Forecasting Heliothis Populations Light- and Pheromone-Trap Catches

We are now monitoring the populations of H. armig- We also monitor H. armigera populations through era across areas and seasons in the hope that we catches of moths in light and pheromone traps.

Cereals Groundnut P i g e o n p e a C h i c k p e a

1 2

1 0

J u l y A u g S e p t O c t N o v D e c J a n F e b M a r A p r

Figure 1. Populations of Heliothis armigera larvae on crops in the pesticide-treated areas of ICRISAT Center, mean data of 1979-80 and 1980-81 seasons.

387 Three light traps have been operated at ICRISAT adequate control of H. armigera and good profits. Center since 1977, the first having been commissi• Endosulfan sprayed at 0.07% concentration in 600 oned in 1975. We intend to analyze the catch data liters of spray liquid per hectare is the most wide • in combination with climatic data in an attempt to spread recommendation. In our surveys, however, determine the factors that are of importance in we found that of the few farmers who used pesti• inducing the large fluctuations in populations. We cides, almost all used DDT and/or BHC, usually as think that there is a probability that there are large- dusts. scale migrations of H. armigera moths across India. The failure to utilize the widely recommended To gain evidence for this, we have joined the Indian endosulfan sprays can be largely attributed to the Council of Agricultural Research in a project in cost and nonavailability of this pesticide and a which light traps have been set up to monitor H. shortage of water during the flowering and podding armigera in several centers throughout the country. period. Moreover, most genotypes of pigeonpeas Some centers have found the maintenance of light that are grown by farmers reach a height of more traps difficult or impossible where no electric pow e r than 1.5 m at the time of flowering, and the applica• is available, and sorting light-trap catches is a tion of pesticides to such crops is difficult, particu• skilled and time-consuming process. We have also larly with the applicators that are available to initiated a network of pheromone traps, baited with farmers in India at this time. There appear to be two rubber septa impregnated with the synthetic H. ways of dealing with this problem: to reduce crop armigera pheromone, developed and supplied by height or to develop spraying methods with the Tropical Products Institute (Nesbitt et al. 1979, machinery that can give adequate coverage to tall, 1980) with whom we are in active cooperation. dense crops. Our breeders are now attempting to These pheromone traps have obvious advantages develop genotypes that are small but productive. over light traps for they are relatively cheap, require We are also looking at alternative methods of pesti• no power source, and almost all catches are of H. cide application, including the use of controlled armigera male moths, so little time is wasted in droplet applicators (CDA) and have found marked sorting the catches. improvement in pest control by using these spray• We are now well into a project comparing the two ers. At present neither the CDA equipment nor the types of trap catches with each other and with low volatile pesticide formulations required for this counts of eggs and larvae from the plant hosts method are readily obtainable in India. across ICRISAT Center. If we find that the trap The application of pesticides to chickpea is rela• catches can give reasonable estimates of pest tively easy, but the profits from pesticide use in populations we should be able to help the Indian most areas and years appear to be much lower national entomologists who are participating in the than those from pesticide use in pigeonpea. Repli• trap network to identify the factors, including mig r a • cated comparisons of pesticide-protected and tion, that determine the populations of this pest in pesticide-free chickpea plots from 1977 to 1981 their areas. Pheromone traps may also be of use as showed yield increases ranging from 8.7% to 50%, indicators of the need for pesticide use against H. with a mean increase of 28%. This is in sharp armigera on crops in a district. We also intend to contrast to the benefits obtainable from the use of investigate the possible role of pheromones in pesticide on pigeonea, on which we often record reducing H. armigera populations in an area using gains of more than 200%. The average yield either a mass trapping or a confusion technique. increase produced by pesticide use on pigeonpea at ICRISAT over all seasons, maturities, and fields has been more than 100%. Work on Heliothis Control

Natural Control Elements Pesticide Use We have been monitoring the natural control ele• Our surveys of farmers' fields revealed that only m e n t s of H. armigera and other pests on pigeon• 5.9% of pigeonpea fields and 7.3% of chickpea pea, chickpea, and other crops and plants fields were treated with pesticides. Intensive work throughout each year, both at ICRISAT Center and by the All India Coordinated Pulse Improvement in farmers' fields. Although no virus particles cou l d Project has shown that several pesticides can give be detected in samples of dead larvae collected

3 8 8 from our fields a n d sent to the B o y c e T h o m p s o n era in south-central India have so far revealed 27 Institute (BTI) for analysis, we a r e frequently species of insect parasites (Table 2). troubled by nuclear polyhedrosis virus (NPV) epi• In addition, we have also recorded at least eight demics in our laboratory cultures of Heliothis spp. hyperparasites from cocoons of the Campoletis / In 1 9 7 7 - 7 8 , in collaboration with BTI, we undertook Diadegma parasite complex that are commonly preliminary field tests of sprays containing NPV, found on H. armigera. originating from a culture supplied by the T a m i l We have m a d e a few observations on the p red a - Nadu Agricultural University. These tests showed tors of H. armigera a n d have n o w d e c i d e d that this that we could a c h i e v e considerable mortality (up to aspect requires increased attention. We h a v e 60%) of H. armigera larvae on c h i c k p e a , using high recorded 19 species of insects preying upon e g g s d o s a g e s of the virus. Since t h e n we have m a d e no and larvae of H. armigera a n d suspect there are further attempt to develop this a p p r o a c h , for we c a n many more. We also consider that other groups of see no practical future for the use of m i c r o o r g a • predators, particularly birds and spiders, can be of nisms in pest control until the national regulatory importance in reducing H. armigera populations. bodies develop a defined practical attitude to their Our studies of the natural enemies of H. armigera development and utilization. have revealed a complexity of species-crop- Mermithid n e m a t o d e s are very c o m m o n paras• season interactions that must be understood, or at ites of Heliothis spp larvae collected early in e a c h least recognized, for such knowledge is essential season, particularly from weed hosts in unculti• before we embark upon attempts to a u g m e n t t h e vated grazing areas on Alfisols within 50 km of natural control of this pest. For example, of nearly ICRISAT Center. In one case, 9 3 % of 302 Heliothis 12 000 eggs of H. armigera collected from sorghum spp larvae collected in August w e r e parasitized by from August to October, 1978 to 1980, m o r e than nematodes. This parasite, w h i c h has bee n identi• 2 5 % were parasitized, but of more than 9 0 0 0 eggs fied as Ovomermis albicans, has been f o u n d in collected from pigeonpea from September to Feb• larvae of H. armigera, H. peltigera, a n d H. assulta. ruary, 1978 to 1 9 8 1 , less than 0.1 % were parasit• Unfortunately, it does not persist through the sea• ized. We have also found that most parasites son, for f e w are found after September, w h i c h is the recovered from H. armigera larvae on s o r g h u m are mo n t h w h e n H. armigera starts to attack our pulse Hymenoptera, while those collected from larvae on crops. pigeonpea are predominantly Diptera (Table 3). Our surveys of t h e natural e n e m i e s of H. armig- T h e identification a n d quantification of t h e n a t u -

Table 2. Parasites that have emerged from eggs, larvae, and pupae of Heliothis a r m i g e r a collected from Andhra Pradesh, Maharashtra, and Karnataka states ln India .

D i p t e r a Hymenoptera

T a c h i n i d a e B r a c o n i d a e B e t h y l i d a e c Carcelia illota Apanteles spc Gomozus sp Exoristis xanthaspis Bracon spc Ichneumonidae Goniophthalmus h a l l id Chelonus spb Barichneumon spd c Palexorista laxaa Microchelonus Campoletis chlorideae Pale xorista s o l e n n i sc curvimaculatusb Diadegma spc Palexorista spc Rogas sp Enicospilus s h i n k a n u s d Sturmiopsis i n f e r e n s c Trichogrammatidae Eriborus argenteopilosus Trichogramma chilonisa Eriborus t r o c h a n t e r a t u sc Trichogramma spa Ichenumon spc Trichogrammatoidea spa Metopius rufusc Trichogramma to idea Temelucha sp bactrae sp fumata a Xanthopimpla s t e m m a t o rc a = parasite of egg; b = egg-larva; c = l a r v a ; d = larva ex-pupa

3 8 9 Table 3. Parasitism levels recorded from eggs and larvae of Heliothis a r m i g e r a on sorghum (CSH-6) and pigeonpea (ICP-1) in cropping systems trials at ICRIS AT, 1978-81.

Pest Collection N o . o f H . armigera Parasitism (%) s t a g e p e r i o d s C r o p e x a m i n e d Diptera Hymenoptera

E g g s A u g - O c t S o r g h u m 1 1 8 4 6 0 . 0 2 6 . 4 Sept-Feb Pigeonpea 9 2 5 0 0 . 0 0 . 1

Larvae Aug-Oct Sorghum 6 0 9 8 2 . 1 2 4 . 9 Sept-Feb Pigeonpea 1 4 0 5 2 1 0 . 2 1.1

ral control elements of H. armigera, at and around confirm or deny the importance of migration in this ICRISAT, has been an interesting exercise. How• species. ever, it is of no direct value in furthering our aim of enabling the small farmer of limited means to pro• Augmentation of Natural Control duce more food from his land. But we regard such surveys as prerequisites to augmenting natural Our research on augmentation of natural enemies control levels and to minimizing damage to natural is still in its preliminary stages. We will examine the control agents where pesticides are used. potential for augmentation of the natural control elements both native and exotic. From 1979 we have been gaining experience in the handling, breeding, and release of the tachinid fly, Eucelato- Effect of Pesticides on Heliothis ria sp, which was imported from the United States and on Natural Control Elements by the Plant Protection Directorate of the Govern• ment of India. We have found that the laboratory At ICRISAT Center we normally use endosulfan to breeding of this parasite, using both laboratory- r e d u c e H. armigera populations, for this pesticide is bred and field-collected H. armigera as hosts, has generally considered to be less damaging to the been relatively easy. Field-cage releases have Diptera and Hymenoptera, which form the bulk of shown that it parasitizes H. armigera larvae feeding the natural enemy complex. In comparisons of H. on pigeonpea more readily than those on chickpea. armigera collected from pigeonpea and chickpea We suspect, however, that this parasite might not from the pesticide-free area of ICRISAT Center and be able to survive the hot dry season at ICRISAT, those from pesticide-protected fields, we have when maximum shade temperatures exceed 40°C found no great or consistent effects on the percen• and unshaded soil surface temperatures exceed tages of larvae containing parasites. However, col• 50°C, for this fly has not survived temperatures lections of H. armigera larvae from farmers' exceeding 35°C in our laboratory tests. We are now pigeonpea in the Tandoor region of Andhra Pra• examining the potential of selecting for tempera• desh, where farmers have used pesticides, particu• ture tolerance in this insect. We also expect to larly DDT, for several years on this crop, revealed a examine the potential of other exotic parasites in very low incidence of parasitism. In addition, there cooperation with scientists within the national pro• are complaints that such pesticides no longer give grams and with the Commonwealth Institute of Bio• adequate control of the H. armigera larvae. There logical Control. We will also be looking for natural are suspicions that populations of this pest may enemies of this pest in India that may be of value if have developed resistance to some pesticides in introduced into other areas, such as eastern Africa. some areas, but there appears to be no recorded The economics of laboratory or "factory" produc• evidence to support this. We are hoping to cooper• tion of parasites that may be candidates for inunda- ate with the Indian Agricultural Research Institute tive release projects will have to be carefully in Delhi in a study of the susceptibility of H. armig• assessed. In most developing countries the labor era larvae, collected from various areas, to pesti• costs are relatively low compared with the USA and cides. This project could also give evidence to Australia, so this may benefit such projects.

3 9 0 Cropping and Cultural Practices in the later crop. However, intensive research on this system over the past few years has failed to Our surveys revealed that more than 70% of establish such a benefit. If anything, pigeonpea in pigeonpea is grown as an intercrop, the major com• sorghum intercrops appears to suffer greater per• panion crops being sorghum, millet, cotton, and centage damage than is recorded in pigeonpea other legumes. The main reason for this practice sole crops. Data from a series of trials comparing appears to be that pigeonpea grows very slowly for sole crops of sorghum and pigeonpea with inter• the first 2 months after sowing, thus leaving bare crops involving two spacing levels of the two crops ground and an opportunity for weeds to thrive in the are summarized in Table 4. early stages of the monocrop situation. A faster We consider that these data can largely be growing intercrop will help cover the ground quickly explained by the failure of most of the natural ene • and smother the weeds. Many farmers intercrop mies of H. armigera on sorghum to transfer to the sorghum with pigeonpea. Studies of this combina• pigeonpea. We have already shown in Table 3 that tion by the Farming Systems Program of ICRISAT the majority of parasites from H. armigera collected have shown that, given the right plant populations, from sorghum are Hymenoptera, while most of a crop of sorghum almost equal in yield to a mono- those from pigeonpea are Diptera. There also crop can be harvested in October, leaving the inter• appears to be an almost complete absence of par• cropped pigeonpea to grow and spread into the asites in eggs collected from pigeonpea; yet egg space vacated by the harvested sorghum and so parasites are common and may play an important produce a substantial yield of pigeonpea from role on sorghum. Thus, the sorghum/pigeonpea December onwards, according to the maturity of intercrop appears to be an unfortunate combina• the genotype. In this system, land equivalent ratio tion, where the pest transfers from the earlier to the (LER) yields of greater than 1.4 have been com• later crop, but its major natural enemies do not. This monly recorded (in comparison with sole crops). may be in sharp contrast to other intercrops, such It is commonly considered (van Emden and Willi• as cotton/pigeonpea, for surveys of this system in ams 1974) that systems with species diversity will some states showed high levels of dipteran paras• tend to have more stable and robust ecological ites in H. armigera larvae collected from both cot• systems than monocrops. It has been generally ton and pigeonpea, so that there the parasites may assumed that intercropping, particularly where a transfer with the pest. Such interactions are a com • major pest and its natural enemies can thrive on plex of plant-insect-seasonal effects and deserve both the crops in sequence, in a system such as further research. Some details of this work have that provided by the sorghum pigeonpea intercrop, been published by Bhatnagar and Davies (1980), should give benefit to the buildup of natural ene• and more complete data are provided in ICRISAT mies and consequently to suppression of the pest Annual Reports and in departmental progress

T a b l e 4 . C o u n t s o f H e l i o t h i s a r m i g e r a, percentage yield loss, and yields of pigeonpea grown a s m o n o c r o p a n d Intercropped with sorghum at two spacings (mean data from trials at ICRISAT Center, 1978-81).

Heliothis/100 terminals at

peak activity Y i e l d G r a i n y i e l d s ( k g / h a ) LERa C r o p Eggs Larvae l o s s (%) P i g e o n p e a S o r g h u m

Sorghum monocrop 2 5 4 4 1 . 0 P i g e o n p e a m o n o c r o p 8 5 4 4 3 5 . 9 1 0 4 3 1 . 0 5 4 1 2 0 0 5 Intercrops wide spaced 1 1 1 4 1 3 6 . 6 1 . 4 1 8 0 0 Intercrops close spaced 1 1 0 4 6 3 9 . 3 5 7 5 1 . 4

SE ( m ) ± 7 . 0 3 . 7 2 . 3 3 7 3 . 9 1 8 1 . 1 0 . 1 1 a . L E R = L a n d E q u i v a l e n t R a t i o .

391 reports distributed by the Cropping Entomology situated for open-field screening of genotypes unit of the Farming Systems Research Program at against H. armigera, for in recent years this pest ICRISAT. has appeared in sufficient numbers for screening, In addition to the intercropping studies, we have during the pigeonpea and chickpea seasons. We also experimented with cultural practices in mono- also have unique advantages in this work, for ICRI• crop pigeonpea and chickpea by varying spacings SAT has the responsibility of maintaining the and times of sowings, with cultivars of differing world's germplasm of both crops and has been maturities. All of these studies indicate greater p o p • provided with sufficient funds and staffing to carry ulations of H. armigera larvae per unit area with out intensive and sustained screening programs. greater plant densities in both crops, but with no The problems of screening for resistance to Heli• obvious increase in the percentage damage in the othis spp are obvious. The pest itself is polypha- pods. Typical data are shown in Table 5. gous and so is unlikely to be susceptible to small Our physiologists find marked yield advantages changes in the chemical or physical composition of in close spacing for both these crops, but their any particular host. Plants are not normally results are from pesticide-protected trials. Our attacked until the flowering or fruiting stage so the spacing trials in the pesticide-free areas often screening of large numbers of seedlings, which has show a reduction of yield when pigeonpea is provided quick results in many other pest- and 2 planted closer than five plants/m and chickpea is disease-screening programs, is of little or no utility 2 planted closer than 16 plants/m . for H. armigera. We entered into our screening We have found that sowing dates and/or the use programs with a full awareness of the problems of genotypes with differing maturities can have a involved and a knowledge that the search for res• major effect on the H. armigera infestations attack• istance to Heliothis spp in other crops had met with ing any particular pigeonpea plot. Here at ICRISAT, only limited success. However, we are also aware pigeonpea flowering in November has a severe that most breeding and improvement programs infestation of H. armigera larvae in most years. involving these crops are carried out in environ• Pigeonpea flowering in February has relatively little ments where pesticides are used to protect the attack by H. armigera, but other pests, including the trials. Such programs are likely to produce mate• podfly and a plume moth larva, Exelastis atomosa rials that will be of no use in the real world, where are more damaging at that time. few farmers protect their crops with pesticides. Pigeonpea and chickpea are markedly different in many aspects, and these differences have Screening for Resistance affected the progress in screening for resistance. Pigeonpea is a slow-growing but large plant that is For both pigeonpea and chickpea, which are still susceptible to many pests and can have a high grown without pesticide use in most farmers' fields, percentage of outcrossing. Thus, relatively few the development of selections with reduced sus• plants can be grown per unit area and no more than ceptibility or tolerance to attacks by Heliothis spp one generation of the mid- and late-maturity types could lead to enormous benefits. ICRISAT is ideally can be grown per year. In open-field screening we

T a b l e 5 . H e l i o t h i s armigera larvae recorded per m2 and percent pod damage In plant-density trials at ICR ISAT Cantar, 1978-1979.

P i g e o n p e a C h i c k p e a Plants/m2 M e a n n o . P o d s d a m a g e d Plants/m2 M e a n t o t a l P o d s d a m a g e d 2 2 H. armigera/m (%) H. armigera/m (%)

1 . 4 2 . 6 2 4 3 . 3 1 3 . 5 1 8 4 . 4 4 . 0 3 0 8 . 0 2 0 . 3 1 9 1 0 . 7 5 . 2 2 5 3 3 . 0 4 8 . 7 1 9 6 7 . 0 5 1 . 4 2 4 SE ( m ) ± 0 . 1 7 ± 1 . 2 ± 0 . 9 8 ± 0 . 3

3 9 2 cannot determine whether any line or plant has any quickly replace these with a second flush that can resistance until the podding stage, and even then give an equal or greater yield. This complicates our resistance to H. armigera may be masked by the testing, for we now routinely record both the first- damage caused by other pests. The seed from and second-flush yields, and the pod damage in selected plants is likely to have been outcrossed, these, from each of our many trials. Data from one so that we are dealing with a segregating mess in such trial are shown in Table 6. subsequent generations. Attempts to utilize field In this trial we used balanced lattice squares, a cages in which the infestations of Heliolhis c a n be design that we have found to give substantial controlled, as used by Lukefahr et al. (1975), have advantage in efficiency for such testing, when not been successful at ICRISAT. compared with randomized block designs. We In spite of all these problems, we have made have found several lines that show consistent dif• some progress in screening for resistance within ferences in their susceptibility to pest attacks an d the available germplasm. We have developed a some that consistently give reasonable yields in methodology (Lateef and Reed 1980) that first spite of heavy pest attacks. However, we have not rejects the most obviously susceptible materials in yet selected any plants that are outstandingly res• unreplicated screening and then progresses to istant to H. armigera attacks, and two or three pesti• replicated testing of materials, against appropriate cide sprays during the flowering period will usually checks, within trials that each contain a narrow result in very large increases in yield from all of our range of maturities. This is essential, for the inclu• early and mid-maturity selections. sion of plants with differing maturities in any trial will We have found that some of the Atylosia spp, simply result in the selection of plants that happe n which are close relatives of pigeonpea, have con• to flower and pod during a dip in the pest population siderable resistance to H. armigera a n d other pressure! pests. Feeding tests have shown that A.scara- We have tested over 10 000 germplasm acces• baeoides has marked antibiosis, for H. armigera sions and breeding lines and have selected mate• reared on this plant show increased mortality, pro• rials in each maturity group that have shown more, longed larval periods, low pupal weights, and and less, resistance, and also those that are toler• reduced fecundity. This plant can be crossed with ant to H. armigera and other pests. Some pigoen- pigeonpea, and, in cooperation with our breeders, pea plants have an outstanding ability to we now have several selections from the deriva• compensate for losses to pests; all of the first flush tives of such crosses that are of some interest, of flowers or pods may be lost, but the plant can including entries 6 and 7 in Table 6.

Table 6. Percentage of pods bored (mainly by H. armigera) and yields from a balanced lattice-square design trial of pigeonpea selections In the pesticide-free area of ICRISAT Center, 1980-81.

F i r s t p i c k Second pick T o t a l B o r e d Plota B o r e d P l o t y i e l d E n t r y G e n o t y p e p o d s ( % ) y i e l d ( g ) p o d s (%) y i e l d ( g ) ( k g / h a )

1 P P E - 4 5 - E 2 1 7 . 2 5 5 1 1 4 . 2 1 1 5 8 0 0 2 S e h o r e 1 9 7 2 9 . 1 8 5 8 3 5 . 0 1 0 9 1 1 6 0 3 T-21 (Check) 3 3 . 7 7 0 6 1 8 . 9 1 2 2 9 9 3 4 ICP-7349-1-S4 3 0 . 1 6 9 7 1 7 . 5 1 4 5 1 0 1 1 5 ICP-7203-E1 2 6 . 9 9 4 1 1 8 . 7 2 5 8 1 4 3 8 6 1914(IG)-E2 1 5 . 5 6 0 7 2 0 . 6 1 5 0 9 0 9 7 1925(IG)-E2 2 6 . 6 8 1 7 1 0 . 1 1 5 5 1 1 6 6 8 I C P L - 1 0 0 2 2 . 0 5 8 5 2 2 . 4 1 6 4 9 0 0 9 ICP-1903-E1 1 3 . 0 8 0 2 1 4 . 9 1 5 6 1 1 5 0

S E ( m ) ± 3 . 0 4 8 . 2 4 . 2 5 2 9 . 3 9 2 . 1 C V (%) 2 5 . 6 1 3 . 2 4 2 . 5 3 8 . 5 1 7 . 2 a . Net plot harvested = 8.33 m2 .

3 9 3 In cooperation with our biochemistry unit and with appropriate checks. In this way we have with the Max-Planck Institute for Biochemistry in screened all of the available germplasm and the Munich, we have initiated studies of the factors breeders' and pathologists' materials, making a involved in resistance or susceptibility to pests in total tested of more than 12 000 lines. this crop. This work is in an early stage, but several Early-maturing chickpeas yield better than those interesting chemical and physical differences have of later maturity at ICRISAT Center but generally been observed. suffer from the heaviest H. armigera attacks, partic• Chickpea is a rapidly growing, but small, plant ularly at the podding stage. It is within this grou p that is almost invariably self-pollinated and has a that we have had our greatest success, for we have remarkably restricted range of insect pests. How• been able to select lines that are consistently less ever, this crop is particularly attractive to H. armig• attacked than the commonly grown cultivars, and era from the seedling stage. This is illustrated in also yield more in pesticide-free conditions. Data Table 7, which summarizes the egg laying on both from a 1980-81 balanced lattice square design chickpea and pigeonpea grown in pots and trial, which was carried out in cooperation with our e x p o s e d to H. armigera moths in field cages. These breeders, are shown in Table 8. data show that although pigeonpea is more attrac• Here we grew four of our best selections together tive from the flowering stage, chickpea is outstand • with four entries that the breeders had selected in ingly attractive to egg laying during the vegetative their pesticide-protected trials, and a well-known stage. cultivar as a check. It can be seen that the entries Chickpea can be eaten down to bare stalks by H. previously selected as being less susceptible to H. armigera larvae during the vegetative stage, but will armigera showed less damage and greater yields usually recover to give a crop, provided there is than the other entries. There was a similar trial sufficient moisture in the soil and the temperatures under pesticide protection, but there we had a are not t o o high. heavy incidence of fusarium wilt, and the best of Although the chickpea plant differs considerably our selections were susceptible to this disease. from pigeonpea, we have found that the general Our breeders have been crossing our selections methodology developed for the field screening of with wilt-resistant materials and the progenies of the latter is equally effective for the former. On these are being selected in wilt-sick plots in this chickpea we record the damage at the seedling season. The seed of our best selections has been stage, the percentage pod damage, and the yields, made available to the national scientists, and the and use all three criteria in our selection. preliminary results from tests in southern India are Our initial screening is in unreplicated small promising. plots. Here the major problem is with uneven distri• We have not been so successful in selecting for bution of populations of H. armigera larvae in s p a c e resistance to H. armigera in the later maturing and time, which allows chance escapes from dam• chickpeas which yield well in the major chickpea- age. In this initial screening we discard the entries growing tracts of northern India. We have recently that appear to be very susceptible. Subsequent transferred much of our selection and testing of this tests are with increasing replication of the entries, group to the farm of the Haryana Agricultural Uni- which are grouped into narrow maturity categories, versity at Hissar, where the later maturing chickpeas yield well and are also subject to heavy H. armigera attacks.

Table 7. Mean numbers of eggs laid on chickpea and pigeonpea plants grown In pots and exposed to H. armigera moths in field cages at ICRISAT, 1978-79. Mechanisms of Resistance

Mean no. of eggs laid/plant In cooperation with our biochemistry unit and with the Max-Planck Institute of Biochemistry in S t a g e Chickpea Pigeonpea Munich, we are studying the mechanisms of resist• a S e e d l i n g 12.5(120) 2 . 3 ( 1 3 4 ) ance or susceptibility of pigeonpeas and chick- F l o w e r i n g 1.2(113) 18.5(105) peas to H. armigera attacks. The green tissues of chickpea plants are densely covered with glandu• a . Figures in parentheses are number of lar hairs that exude very acidic (pH 1.3) droplets; plants examined. this very acid exudate is probably what deters most

3 9 4 Table 8. Comparison of entomologists' and breeders' selections of early-maturing chickpeas in pesticide-free conditions at ICRISAT Cantor, 1980-81.

Mean p o d Y i e l d G e n o t y p e S e l e c t e d damage ( k g / h a ) (%)

a IC-7394-18-12-1P Ent 14.6 2223 I C C - 5 0 6 Ent 5.1 2001 IC-738-8-1-1P Ent 9.9 1963 IC-73103-10-2-1P Ent 14.9 1900 b I C C C C - 9 Br 18.0 1876 Annigeri-1 (check) - 20.0 1828 I C C C - 6 Br 17.8 1726 I C C C - 8 Br 14.9 1685 I C C C - 1 Br 28.0 1297

SE (m) ± 1.70 4 7 . 0 C V % 2 1 . 3 5.1

a . Ent = Selected by entomologists in pesticide-free fields in previous seasons. b . Br = Selected by breeders in pesticide-treated fiel ds in previous seasons.

insect pests from feeding upon this crop. It has These tests have given variable results, but it does been shown that some of our more resistant selec• appear that the moths can feed upon malic acid tions tend to have greater concentrations of malic solutions. acid in their exudates (Rembold and Winter, these Proceedings). In addition, the seed of ICC-506, one Integrated Management of the most resistant selections, has a higher con• centration of polyphenols in its seed coat than has Trials combining some of the elements of inte• any other seed so far tested (Umaid Singh, unpub• grated management of H. armigera are already lished). There is a possibility that some of our being field tested at ICRISAT Center. For example, selections may have differing mechanisms of res• we are testing the utility of the more and less istance; our breeders have been crossing the susceptible chickpea selections in pesticide- selections, hoping to produce progeny that have protected and pesticide-free plots, and include multifactor and increased resistance. parasite release and protection from predators in We are particularly interested in finding out what some of these. However, the major elements of any stimulates H. armigera to lay eggs on chickpea pest management program cannot be adequately during the seedling stage, for on most other hosts tested at a center such as ICRISAT, where combi• egg laying is mainly restricted to the flowering nations of crops, sowing dates, and pesticide use stage. One possibility is that the moths are primarily all result in an atypical pest situation. We must carry attracted to plants to feed, usually upon nectar. our experimentation to farmers' fields where we This would explain why there is some egg laying on can encourage the synchronous sowing of crops cotton before flowering, for on that crop the extra- that will limit the buildup of H. armigera in the area floral nectaries on the leaves could provide food. and also dilute the populations that will occur. Th e On chickpea there is a possibility that the moths use of pesticides and natural enemy augmentation can feed upon the acid exudate. We have been will also be controlled over the area. We anticipate conducting laboratory tests comparing the oviposi- that we will be in a position to suggest such experi• tion of moths that are allowed access to honey, mentation within the next 3 years, in cooperation differing concentrations of malic acid, and water. with national agencies.

3 9 5 Summary

Research towards the effective and economic management of insect pests, but particularly H. armigera, has been in progress at ICRISAT for the last 7 years. Our early work was largely concerned with determining the basic data of the incidence of the pests and their natural enemies on the crops, with investigating the biology and ecology of the insects, and with developing the methodology of sampling and screening for resistance to the pests in pigeonpea and chickpea. We are now well into the action phase of our research, where we are investigating the possibility of improving the ele• ments of pest management on these crops, includ• ing economic pesticide use, natural enemy augmentation, and the use of less susceptible and more tolerant plants. We soon hope to test our findings in farmers' fields, through the national a g e n c i e s .

References

BHATNAGAR, V.S., and DAVIES, J.C. 1980. E n t o m o • logical studies in intercropped pigeonpea systems at ICRISAT Center: future developments and collaborativ e research needs. Pages 341 -347 in Proceedings, Interna• tional Workshop on Pigeonpeas, Vol. 2. ICRISAT/ICAR , 15-19 Dec 1980, Patancheru, A.P., India.

LATEEF, S.S. and REED, W. 1980. Development of a methodology for open field screening for insect pest r e s • istance in pigeonpeas. Pages 315-322 in Proceedings, International Workshop on Pigeonpea, Vol. 2. ICRISA T/ ICAR, 15-19 Dec 1980, Patancheru, A.P., India.

LUKEFAHR, M.J., HOUGHTALING, J.E., and GRUHM, D.G. 1975. Suppression of Heliothis spp. with cottons containing combinations of resistant charact e r s . Journal of Economic Entomology 68(6): 743-746.

NESBITT, B.F., BEEVOR, PS., HALL, DR., and LES• TER, R. 1979. Female sex pheromone components of the cotton bollworm, Heliothis armigera. Journal of Insect Physiology 25:535-541.

NESBITT, B.F., BEEVOR, P.S., HALL, D.R., and LES• TER, R. 1980. Hexadecenal: a minor component of the female sex pheromone of Heliothis armigera ( H u b n e r ) (Lepidoptera, Noctuidae). Entomologia Experimentali s e t Applicata 27:306-308.

REMBOLD, H., and WINTER E. 1981. The chemists role in host-plant resistance studies. Session 5, t h e s e Proceedings.

VAN EMDEN, H.F., and WILLIAMS, GF. 1974. I n s e c t stability and diversity in agro-ecosystems. Annual R e v i e w of Entomology 19:455-475.

3 9 6 Discussion—Session 7

This discussion concentrated upon three aspects NPV a n d Bacillus thuringiensis have not been util• of Heliothis management. ized by most farmers in Australia or the USA, but 1. The pest status of Heliothis spp on different there is a market for these. Although the use of crops, particularly, of the increased activity parasites and predators does not appear to be an of these pests with changes in cropping patt• active component in many Heliothis management erns and practices. schemes, the records of natural enemy abundance 2. The current advances in management of are often taken into account when taking decisions these pests with improved technology. on pesticide use. 3. The problem of insecticide resistance and The Chairman closed the discussion with the the prospects for new pesticides. There is remark that the integrated package still appears to great concern that Heliothis spp may quickly be a limping package in most areas. We have a build up resistance to new insecticides as a long way to go before we replace the total reliance result of cross resistance resulting from the upon chemical pesticides with a realistic integrated older insecticides. management approach in most areas.

397

Session 8

Prospects for Future International Cooperation

Chairman: J.C. Davies Rapporteurs: P.W. Amin Cochairman: G. Hariri S. Sithanantham

Prospects for Future International Cooperation

This session consisted of a series of discussions Behavior Studies concerning the subjects covered in the previous sessions. Discussion leaders reviewed each of It was agreed that practicable pest-management those sessions, introduced the potential areas of strategies must be based upon an adequate knowl• cooperation for general discussion, and subse• edge of behavior of the pests, and that the present quently formulated recommendations for future availability of such knowledge was inadequate for action and cooperation. A summary of these dis- the Heliothis spp, particularly for H. armigera. Stu• cussons and recommendations follows. dies of moth behavior in the field have been very few and far between, largely because Heliothis moths are nocturnal but man is notl Recent noctur• Session 1: Biology, Behavior, nal studies of both H. virescens a n d H. zea in the and Ecology of Heliothis USA have been extremely productive, and it was suggested that ICRISAT should now embark upon Discussion leader: P. D. Lingren similar studies for H. armigera. The availability of image intensifiers in night-vision equipment has Subspecies Identification given some impetus to the nocturnal studies. How• ever, a great deal of information on emergence It has been generally agreed that H. armigera is a patterns, population aging, feeding, mating, and single, polyphagous species extending over much trivial movement of moths can be obtained by using of the tropical and temperate areas of the world, head lamps. The belief that all Heliothis nocturnal with the exception of the Americas, where H. zea behavior is so disrupted by artificial illumination replaces it. However, it is probable that there are that observations using artificial lights are useless, differences between the H. armigera populations of is not justified, for when a moth enters a particular different areas that merit race or subspecific rank. behavioral activity it is not readily diverted from that Such differences are of importance where they activity by a head lamp that is just powerful enoug h involve the host range, aestivation-hibernation- to permit easy observation. diapause abilities, other biological factors, and s u s • There is also a need for further studies of the ceptibility to pesticides. At this time there appears behavior of the Heliothis spp larvae during both the to be little well-documented knowledge of such day and the night. Such studies would provide use• differences. ful information for the improvement of most ele• It was suggested that the identification of sub- ments of control strategies, but particularly for species of H. armigera and the geographical range host-plant resistance and pesticide use. of these might be partially accomplished by the use of electrophoresis. Although this technique is fairly expensive, it is simple and straightforward. It was Aestivation and Diapause suggested that either the live insects or acetone- extracted materials should be sent to a central Studies of H. virescens and the sterile hybrid in laboratory for testing. The advantage of sending Arizona have revealed that it is fairly easy to induce live insects to a central laboratory would be that a period of aestivation with high temperatures. In comparative biological tests could also be done. Australia and the Sudan there is also some evi• For quarantine reasons, such a central testing dence for the occurrence of aestivation in the pre- laboratory would have to be situated in a country pupa but more commonly in the pupal stage. It was where Heliothis spp are not a threat to the local suggested that some of the observed anomalies of agriculture. The United Kingdom was suggested as the occurrence of H. armigera moth populations in a suitable location. peaks might be explained by the presence of aesti-

401 vating pupae that e m e r g e in s y n c h r o n y w h e n c o n • 3. Electrophoresis should be used on extracts of ditions are favorable after a hot period or a drought. adults a n d larvae from various areas in an attempt T h e o c c u r r e n c e of diapause in H. armigera, par• to distinguish races a n d s u b s p e c i e s of the Heliothis ticularly of diapause in Asia, d o e s not a p p e a r to be spp that cannot be distinguished by morphological well d o c u m e n t e d or understood. T h e r e is a need for characters. This could be in conjunction with, or laboratory a n d field observation of the o c c u r r e n c e followed by, cro ss-b re e d in g experiments in an of d i a p a u s e a n d of t h e factors that induce and institution in a country that is not threatened by break it. The ability of individuals from differing Heliothis spp. geographical populations to enter diapause is well 4. T h e effect of adult a n d larval food sources on worth studying, for it w o u l d help to d e t e r m i n e the the d y n a m i c s of Heliothis populations requires existence of races and the importance of migration. more research. If, for e x a m p l e , diapause c o u l d be i n d u c e d in a population from o n e area but not f r o m another, this may be g o o d e v i d e n c e that migration plays a rela• tively minor role in the population d y n a m i c s of this Session 2: Surveillance, pest a c r o s s those areas. S u c h a c o n c l u s i o n w a s Forecasting, and Modeling r e a c h e d regarding t h e pink bollworm w h e n individ• of Heliothis Populations uals derived f r o m populations of that pest in south• ern India c o u l d not be i n d u c e d to enter diapause but those from northern India c o u l d readily be Discussion leader: J.R. Raulston i n d u c e d to enter diapause.

T h e discussions during this session revealed that we do not have the capability of predicting the size Effects of Host Plants of Heliothis populations. However, s o m e progress has b e e n m a d e in predicting the timing of Heliothis It w a s a g r e e d that, although there were extensive attacks, particularly in the USA. T h e r e is a clear reports of the effects of various host plants on the need to a s s e m b l e the available information, if only biology of H. armigera, there w a s a need for further to reveal the gaps in our knowledge and h e n c e the studies of f o o d utilization, host preferences, and priorities for future research. effects of larval diet on the fecundity and oviposition p r e f e r e n c e s of the moths. Studies are also required on t h e feeding of m o t h s on different hosts Surveillance a n d the effect of s u c h feeding upon fecundity. T h e polyphagous nature of the major pest species of Heliothis gives special problems in surveying Recommendations populations in alt but m o n o c r o p p e d areas. Counts of eggs a n d larvae on a wide range of crop a n d wild 1. Population-management strategies must be hosts in an area are very expensive in terms of b a s e d on an a d e q u a t e understanding of the behav• recording time and are seldom considered to be ior of the larvae a n d adults of the Heliothis spp. worthwhile. Counts on the individual crops are There is a conspicuous lack of information con• often undertaken for pesticide use decision m a k • cerning the behavior of H. armigera. ICRISAT, in ing, but s u c h counts are seldom useful, or used, for cooperation with scientists from other institutions, population d y n a m i c s studies. We c a n count moths should gather information on the behavior of the in light and p h e r o m o n e traps but we must then m o t h s a n d larvae of this species a n d determine determine the relationship of these c a t c h e s to the h o w external factors, s u c h as the weather, influ• actual field populations. It is already obvious that e n c e s u c h behavior. This work will require e x t e n • the relationship b e t w e e n the c a t c h e s in Heliothis sive nocturnal observations in fields, using white p h e r o m o n e traps and field populations is not s i m • light. S o m e studies may, however, require special• ple a n d direct. ized night-vision equipment. T h e r e is a primary need to standardize traps a n d 2. M u c h m o r e information should be gathered then to use these in fields over a long period, c o n c e r n i n g the diapause a n d aestivation of the recording data not only from the traps but also from Heliothis spp, particularly in Asia a n d Africa. the crops. It should then be possible to c o m p a r e

402 these data, together with climatic records, to deter• Genetic markers may be of use in Heliothis- mine the utility of the traps in the quantitative sur• movement studies. The difficulties encountered in veillance of populations. The current ICRISAT using dyes and other chemicals to mark moths studies, in which data from light traps, pheromone were noted, and it was considered that readily iden- traps, and populations of larvae on all known hosts tifiable variants of Heliothis spp moths should be throughout the year are considered, will be particu• sought and carefully maintained, when found, for larly useful. possible use in migration and other studies.

Movement of Moths Weather Conditions and Pest Outbreaks

The movement of moths plays an important and Weather conditions obviously play a key role in the complicating role in the population dynamics of population dynamics of Heliothis spp, but the indi• Heliothis. Such movement can be at several levels, vidual and combined effects of temperature, rain• ranging from trivial movements within a crop, fall, humidity, and winds on populations have not through movement from crop to crop, to the long- been adequately studied. On-site ground-weather range migration from one area to another. Studies observations are important for the understanding of in the USA have already revealed that Heliothis spp when an insect does what, but we also require a are highly mobile and that there is long-range knowledge of upper air conditions and movements migration of populations in each year. There to help us understand the distribution of the moths. appears to be less evidence of long-range migra• Site meteorological observations need to be put tion in H. armigera and there is a need to determine into a synoptic context, and the local insect popula• whether migration is of importance in the popula• tions must be related to those of much wider areas tion dynamics of this species. in biogeographic studies. Networks of light traps and pheromone traps Ultimately we should endeavour to be able to may provide some evidence of migration. In East accurately predict the occurrence of damaging Africa a network of light traps has been used both to Heliothis populations in time and space, through elucidate migration patterns and to provide an early the use of models that include weather inputs. warning system for control of Spodoptera exempts, an armyworm. That same network also appears to have provided some evidence that H. armigera is a Models migrant, and it may be worthwhile to examine closely the data from those traps where H. armig• Many people have been disappointed with models era moths have been recorded. intended to simulate the population dynamics of Radar has been successfully used to track insects because the predicted values often differ moths in several studies, and this technique is greatly from the observed real-world data. The time expected to be of increasing use. It was emphas• and effort spent in collecting masses of data and ized, however, that such improved technical aids feeding these into a carefully designed program will only be of use if we ensure that our knowledge may yield results that are less accurate than a of the behavior of the insects is also developed well-informed guess. However, this is not a good simultaneously. We should try to determine not only reason to give up modeling; it is simply evidence if, when, and how much migration occurs, but also that there is a need to improve on the model. Usu• why it occurs. The physiologial status of the host ally data are collected first and the modeling is the plants as well as climatic factors are likely to be of last stage in the exercise. There is a good case for importance in stimulating moth movement. How• reversing this procedure. Why not build the model ever, we need more information on the physiologi• first and so determine what data are required to cal status of the moths that determines the extent of drive the model? moth movement. The studies using flight mills may The polyphagous nature of Heliothis, its wide be particularly useful in gathering such information. geographical range, its movements and its wide Already available information on other, well- range of natural enemies make the modeling of the researched migrant insects, including locusts and population dynamics of this pest far from simple. armyworms, should also be of utility in Heliothis However, the models already developed in the studies. southern USA have shown considerable promise. It

4 0 3 was pointed out that we are automatically modeling and preservation of genetic markers of Heliothis mentally whenever we consider populations of spp, that may be of utility in population dynamics Heliothis spp, and the factors that affect these. With and other studies. the ready availability of computers we now have an opportunity to make greater use of the mass of data being collected. One major objective of modeling Session 3: Natural and Biological Heliothis populations is to allow the accurate fore• Control Elements casting of damaging populations on a crop in an area, so that provision for the best strategy of ma n • Discussion Leader: D.J. Greathead agement for that infestation can be planned. For such a purpose, very accurate predictions of the In discussing biological control of Heliothis spp it size of any population may not be necessary but an was generally agreed that these pests present spe• accurate forecast of the timing of the infestation cial difficulties because of their polyphagous and may be of real value. Models already available in mobile habits. The population dynamics of these the USA, utilizing data from pheromone traps, major pest species have not received adequate appear to fufil this requirement. The more sophisti• attention; consequently, the quantitative role of the cated use of models, including studies of the natural control elements has seldom been deter• effects of various management practices on popu• mined satisfactorily. Records showing that X% of lation dynamics, may require models of greater the Heliothis eggs or larvae, taken at a certain time refinement, but these should not be beyond our from a plant host, were parasitized or diseased can capabilities within the next few years if adequate be useful, but we have to determine the effects of manpower and technical equipment can be such levels of parasitism—and of changes in those allocated. levels—on the overall populations of the pest in the same and subsequent generations.

Recommendations Parasitoids and Predators 1. Available information on monitoring systems should be assembled, light and pheromone traps There are numerous natural enemies of the Helio• standardized, and the data from the traps com• this spp. In the absence of pesticides, these, in pared with data gathered from scouting for eggs combination with the other natural control ele• and larvae on the host plants in the areas surround• ments, often maintain Heliothis populations at sub- ing the traps. Such work should be done at ICRISAT economic levels in crops. However, there is for H. armigera. potential for the importation and establishment of 2. Simple models should be developed, based more effective natural enemies, particularly to fill upon these inputs, to structure thinking and to help vacant ecological niches. There is a primary need indicate what other inputs are needed to increase to accumulate the available natural enemy data, the accuracy of the models, with the eventual aim both qualitative and quantitative, and to analyze of sophisticated predictive modeling. these to determine the vacant niches and the 3. Radar technology should be utilized, coupled importations that might be useful in filling them. with nocturnal behavior studies of moths and phy• There have been some transfers of Heliothis para• siological studies of the host plants, to elucidate the sitoids between continents, but without major occurrence and cause of both trivial and long- benefits. This should not discourage us from mak• range movement of moths. ing further introduction attempts, but these should 4. Concomitantly, laboratory studies, including be planned carefully. All too often, introductions flight mill experiments, should be conducted to and augmentation efforts have been made using elucidate the physiological status of the moths that parasitoids that are chosen simply because they triggers such movement. are easily reared and maintained in the laboratory. 5. The possibilities of establishing a central fore• Attempts to augment selected natural enemies casting system utilizing all the available data and (e.g. Trichogramma spp, Chrysopa spp, a n d Euce- predictive models, should be explored. The need latoria bryani) should be based upon comprehen- for adequate meteorological data is stressed. sive technical and economic feasibility studies. In particular, the maintenance of adequate popula- 6. A system should be developed for interchange

404 tions through periods when the Heliothis popula• of predation. Birds are also considered to be impor• tions fall to very low levels must be considered. It is tant Heliothis predators, but here again quantitative already clear that there are strong pest-parasitoid- records are scanty. Most of the needs for more host plant interactions, so there is a need for ento• research on the parasitoids that were discussed mologists to extend their studies to the full range of are also applicable to the predators. plant hosts rather than to confine themselves to a single target crop. The host-finding activity of most parasitoids/ Pathogens predators is affected by the host population den• sity. Chemicals emanating from the host insect The use of pathogens for the reduction of Heliothis and/or its products often serve as cues that aid the populations was considered to be an attractive and natural enemy in host finding and host acceptance. exciting prospect. There is already some commer• When the host insect density is low, released para• cial utilization of Bacillus thuringiensis a n d of a sitoids/predators often leave the target area and nuclear polyhedrosis virus for Heliothis control in do not actively seek the host. This leads to incon• the USA and Australia, but the cost: benefit ratios sistent results from natural-enemy releases. To are not yet very favorable when compared with overcome this problem we need to analyze criti• chemical pesticide use. Sales rely heavily on the cally the host-seeking sequence of the selected nonpolluting reputation of these pathogens and natural enemy and to identify the chemicals that also perhaps on their novelty. From other countries, arrest, retain, and stimulate it to seek the host. We including China, there are several reports of the may then be able to synthesize these chemicals successful utilization of insect pathogens, gener• and evaluate them for use in managing natural ally in noncommercial formulations. These formu• enemy populations. The economic feasibility of lations often use the diseased insect cadavers with augmenting the natural enemies of Heliothis m a y little or no purification of the pathogen. well depend on our ability to mass produce them. It The use of sprays containing the mashed bodies was stressed that vigor and essential behavioral of insects that were killed by pathogens may well characteristics must be maintained during mass be cheap and possibly effective, but it was gener• production. ally considered that such a practice is unlikely to be Although the introduction of exotic natural ene• recommended by most national authorities mies and the augmentation of populations with because of the health risks to man and other mam• mass-reared insects appear to be attractive possi• mals. Although the common insect viruses appear bilities, the protection of the existing natural en e • to be nontoxic to mammals, there is no certainty mies in the ecosystem and the maximization of that other organisms present in dead insects, their utility should be our first concern. The natural including the bacteria, are equally safe. e n e m i e s of Heliothis are often referred to in insect In some countries the existence of an important control guides, but explicit instructions for conse r v • sericulture industry also presents a barrier to the ing these or for making insecticide spraying deci• ready acceptance of insect pathogens in pest sions based on their relative abundance are control. seldom provided. The major barrier to the greater utilization of NPV In general, the parasitoids of Heliothis spp have and of some other pathogens is the relatively short been more extensively recorded and studied than viability period in field use. The degradation of NPV the predators, largely because parasitism can be by ultraviolet radiation is well known, and there are recorded by simple collection of the hosts and adjuvants that will extend the infective period of the subsequent laboratory observation, whereas pre• virus in sprays. However, there is a need for further dator studies require relatively long observations in improvement. The alternatives to spraying include the field for very few recorded incidents. In particu• the use of semisolid baits containing the virus and lar, there have been very few studies of the noctur• autodissemination through the release of infected nal predation of Heliothis eggs, larvae, and moths, larvae (and/or moths) in fields. Some research on and observations on the behavior of the predators these alternatives is required. during the night and day have been inadequate. The NPV of the Heliothis spp appears to be While it is generally considered that spiders may endemic in most areas where these pests are play an important role in Heliothis population found, so there may be no advantage in transferring reduction, there have been few quantitative reports viruses from one country to another unless large

4 0 5 differences in the virulence of the geographical 5. Heliothis spp are often maintained at subeco- strains are reported. In countries such as India, the nomic levels by the natural enemies in most crops. importation of viruses is not encouraged. The mass Where this does not happen, the augmentation of culturing of the viruses and other pathogens will the natural control using periodic releases of native usually require an efficient means of mass cultur• or introduced biological control elements should be ing the Heliothis spp. Methods for efficient mass carefully researched and, if feasible, be culture of this insect are now well established and implemented. were reported at this workshop. The purification of 6. Mass-rearing techniques for natural enemies the pathogens to locally required standards and the should be developed for use in augmentation pro• quality control of the final product will require some grams. For this, the development of artificial diets experimentation, but methodologies and expe• and in vitro rearing may be required to ensure rience are already available. economic returns. It was considered that the pathogens are unlikely 7. The behavior and host-seeking sequence of to become the sole means of Heliothis control but selected natural enemies should be critically ana• will be of use in combination with other elements, lyzed, and chemicals that arrest, retain, and stimu • particularly with some degree of host-plant resist• late host-seeking should be isolated and identified. ance, natural-enemy augmentation, and possibly These chemicals should then be synthesized and with chemical pesticides. evaluated for their potential in managing natural enemy populations. 8. Information on the safety of microbials, both to Recommendations mammals and to beneficial insects including silk• worms, should be accumulated and be supple• 1. The potential should be examined for setting up mented by further research where needed. an informal international working group that will National authorities should be encouraged to take consider the biological control of Heliothis spp on decisions on utilization of microbials in pest man• an international basis, exchange and accumulate agement, based upon the safety precautions found natural enemy data, consider the need for the necessary and the potential economic feasibility of exchange of natural enemies between countries their use. and continents, and disseminate information. 9. Further research is required on the evaluation of 2. The identification, quantification and ecological factors that cause the inactivation of microbials in study of the natural enemies of Heliothis spp should field use and the means of overcoming these. be expanded, and the data summarized on a global 10. Where a microbial appears to offer safe, eco• basis. The quantitative effect of the natural ene• n o m i c potential for Heliothis management, an mies on the population dynamics of Heliothis spp experimental pilot plant for its production should be needs to be determined. set up. There would appear to be economic advan• 3. Importations of exotic natural enemies should tages in developing countries, where labor is rela• be carefully planned, using the following criteria; tively cheap. Subsequent studies should involve the imported natural enemy should (a) occupy a application techniques, with careful monitoring of vacant niche, (b) be adapted to the target field cr o p effectiveness, particularly on the overall Heliothis or to important alternative hosts, (c) possess toler• populations in an area. ance to the commonly used pesticides. Other crite• 11. Since microbial use is most likely to be effec• ria normally used for selection, such as adaptation tive when combined with other elements of pest to the climatic conditions should, of course, also be management, studies of interactions, for example considered. with resistant crop cultivars and differing cultural 4. The quantitative effects of specified levels of practices, should be given priority. natural enemy abundance on Heliothis populations should be determined and these data then be util• Session 4: Chemical Pesticides— ized in pest-control decision making. Techniques should be developed for the rapid assessment of Their Uses and Abuses natural enemy populations in selected crops. Con• Discussion Leader: P.H. Twine trol guides should consider the natural enemy pop• ulations, as well as pest density, indecision making This discussion inevitably revealed a divergence of for pesticide use. opinion on the role of pesticide use in Heliothis

406 management. While it was agreed that there have Because of the wide array of social and agricul• been several cases where the use, or perhaps tural systems for which pesticide use is applicable, misuse, of chemical pesticides has resulted in the it is necessary to evolve programs of pest manage• increase of Heliothis and other problems in the ment, including pesticide use, that are specific to longer term, there are also many examples where each circumstance. It was in the appreciation of the careful use of pesticides has resulted in eco• this diversity that the following recommendations nomic returns without obvious problems. The worry w e r e made. that resistance of Heliothis to pesticides would create a major problem in many areas has been Recommendations alleviated, temporarily, by the production of new effective insecticides, including the synthetic pyre- 1. The development and refinement of scientifi• throids, which give highly effective Heliothis c o n • cally based threshold/action levels for each crop trol. However, the need to combat the resistance situation is of immediate priority in helping to mi n • menace remains a top priority. imize the reliance on chemical pesticides. The need for establishing economic threshold 2. In order to improve the contribution of chemical levels for pesticide use, based upon scouting and pesticides to Heliothis management, more efficient other methods of pest population detection, was methods of pesticide application, for both aerial accepted as a priority. On many crops the thre• and ground-based systems, should be developed shold turns out to be unexpectedly high, particu• and research in this area encouraged. larly in crops that can compensate by further 3. Reducing potentially damaging populations by growth. It was also agreed that the populations of aiming the chemical pesticide at the life stage of the natural enemies need to be considered in the the pest that results in the most efficient use of the decision making. chemical and the least effect on nontarget orga• It was agreed that pesticide use should be consi• nisms is a strategy that should be further dered as one element of a pest-management pro• investigated. gram and not as the sole response to Heliothis a n d 4. The full spectrum of chemical pesticides availa• other pest infestations. However, in many of today's ble for Heliothis control in each crop should be agricultural systems, Heliothis populations regu• evaluated in terms of the lowest effective rates, larly exceed established thresholds in crops. In their influence on beneficial species, and the pesti• such circumstances few farmers see any alterna• cide resistance buildup, in order to recommend the tive to chemical pesticide use, particularly in the most appropriate management strategy. less developed countries. 5. Because of the continuing threat of pesticide The inefficiency of the present means of cover• resistance in areas where pesticides are used ing plants with pesticide to kill the pests, rather than intensively, it is suggested that resistance-testing using a much smaller amount of pesticide directed programs be set up to monitor changes in suscepti• at the pest as a target, was appreciated. It was bility values. agreed that the possibility of treating the Heliothis 6. Farmer education programs should be encour• moth as a target is worth further experimentation. aged to facilitate the acceptance of the pest- The treatment of individual fields, rather than syn• management approach and the associated use of chronized efforts to reduce the Heliothis population chemical pesticides within this system. of an area, was also recognized as a constraint that 7. The implementation of other pest-management needs to be overcome. elements can usually be most profitably and prac• There is still a great need to improve application ticably considered as adjuncts to insecticide use techniques, whether the target be the crop or the rather than as total replacements. insect. The development of controlled-droplet application machinery and techniques is regarded Session 5: Host-Plant x Heliothis as a significant advance that is particularly relevant Interactions and Resistance to the semi-arid areas, where the nonavailability of water often precludes conventional spraying. The Screening increasing use of spraying at night was also noted Discussion Leader: A.C. Waiss with favor. (The need for moth behavioral studies to help to improve the efficiency of such spraying was In these discussions it was agreed that the commented upon in an earlier session.) development of plant resistance to Heliothis spp is

4 0 7 one of the most attractive management options, but and perhaps help to identify the mechanism of there were widely varying degrees of optimism resistance. In general, behavioral and biological concerning the potential for this approach. In cash studies will precede genetic and biochemical crops the relatively easy and profitable chemical studies. pesticide option has tended to relegate plant resist• The need for efficient mass-rearing facilities for ance to a relatively minor position. There may be a Heliothis spp was stressed. Although there has greater potential for the utilization of resistance / been some success in open-field screening, using tolerance in low-value crops where pesticide use the available natural Heliothis populations, the gen• does not provide an easy and profitable means of eral finding has been that the great variability in pest control. The development of a two-path such populations, in both time and space, has approach, as followed at ICRISAT, was com• greatly hindered the screening programs. A facility mended. Here, the effort is, on the one hand, to to inoculate the plants in fields, screenhouses, an d produce plants that yield particularly well when laboratories may lead to accelerated progress. given purchased inputs, including protection from Although the polyphagous nature of Heliothis pests; on the other, to select plants that are resist• spp would appear to limit the potential for finding ant or tolerant to the constraints, including pests, crop plants that have substantial resistance to this that are present in most farmers' fields. pest—for it can obviously cope with a wide range of There was a debate on the relative merits of physical and chemical differences in its host closed-system and open-field screening. The plants—there is a positive aspect to this. For oligo- available evidence indicated that both methods phagous pests the detection of preferences is of have advantages and disadvantages, depending little utility under the no-choice situation, but for upon the crop and other factors. Methods of Heliothis there is usually a choice, often of noncrop screening will vary from crop to crop and according hosts, so the development of even slightly less to the facilities and manpower available. It is impor• preferred crops may divert a substantial portion of tant, however, to develop screening methods that the Heliothis population to plants where their feed• can be relied upon to discriminate between more ing is of no concern. and less susceptible plants and then to utilize these It was also pointed out that the utilization of crops in a sustained effort to produce resistant/tolerant with quite low levels of resistance may be of major materials, first from germplasm in the preliminary value when combined with other elements of con• stages of the program and then from the crossed trol. Resistant or tolerant cultivars will require differ• materials produced by the breeders using the origi• ent economic thresholds; this will be of particular nal selections. Far too many resistance-selection importance where a tolerant cultivar replaces a programs are half-hearted efforts that stumble into susceptible one. oblivion after 3 or 4 years with the erroneous con• There should be a free exchange of information clusion that there is no worthwhile level of resist• and materials between scientists and countries. a n c e to Heliothis in the crop. Although the species of Heliothis in the USA differ The need for an interdisciplinary approach to from those in Asia and Africa, it is probable that plant resistance was stressed. The entomologists plants found resistant to one species will have at and plant breeders will, of course, be the primary least some resistance to the other. A good start has participants, but there is usually a need for scient• been made in the case of groundnut, where selec• ists of other disciplines, including chemists and tions found resistant to H. zea in North Carolina, plant physiologists. While it may not be essential to USA, are now being tested against H. armigera a n d determine the mechanism of resistance, in some other pests at ICRISAT Center in India. cases such a determination can accelerate pro• Of other plant-pest interactions, most discussion gress, for it is often much easier to screen directly centered around the use of neem extracts. Several for the mechanism rather than to rely upon the scientists in many countries are now investigating insect as a bioassay indicator, particularly for the use of azadirachtin against several pests, single-plant selections in segregating populations. including Heliothis spp. As this chemical has such The importance of behavioral and biological stu• a complex molecule, it is unlikely that it will be dies of the pest in plant-resistance programs was synthesized cheaply, if at all, so the botanical stressed. Such studies may initially help to deter• source will have to suffice. The economics of the mine the stage of the insect that is vulnerable to the use of this material do not appear to have been available variability in the host-plant germplasm thoroughly researched.

4 0 8 Recommendations value in s o m e studies in the USA, w h e r e the data have been used in prediction models a n d have 1. International pest resistance nurseries should g i v e n u s e f u l i n f o r m a t i o n o n t h e t i m i n g o f be established a n d e n c o u r a g e d . infestations. 2. The exchange of germplasm and progress P h e r o m o n e traps have m a n y a d v a n t a g e s over reports between scientists working on plant resist• light traps, particularly in areas w h e r e electricity is a n c e to Heliothis should be encouraged. not readily available or the supply is erratic. If the 3. Standardized screening techniques and mass- c a t c h e s are found to have a recognizable relation• rearing methods should be established a n d ship to moth populations, p h e r o m o n e traps will publicized. form a relatively c h e a p a n d simple basis for net• 4. T h e r e should be a multidisciplinary a p p r o a c h to works or grids of traps over regions, the data from the studies of the genetics and m e c h a n i s m s of w h i c h may be of use in determining the extent of host-plant resistance. migration a n d the relationship of populations to 5. The use of insect repellents, including neem and cropping patterns and climates. Such networks other plant extracts, should receive some attention may also provide us with useful predictive data, in pest-management studies. while arrays of traps within individual crops might be of value in indicating thresholds for pesticide use. Session 6: Novel Methods of T h e duration of the period of attraction of s y n • thetic p h e r o m o n e s has been found to vary c o n s i d • Heliothis Management erably. S o m e have been recorded to lose m u c h of their attraction within a few hours, but rubber septa Discussion Leader: G.H.L. Rothschild impregnated with synthetic p h e r o m o n e of H. armigera, formulated by the Tropical Products T h e discussion in this session c o n c e n t r a t e d upon Institute of London, have exhibited considerable the potential use of pheromones and sterile hybrids attraction for up to 3 months of exposure in traps at of Heliothis. ICRISAT, with little or no reduction of c a t c h e s dis• cernible over the first month of exposure. Attrac- Pheromones tants of s u c h longevity are of obvious utility in trap networks. T h e r e has been a considerable improvement in the T h e use of p h e r o m o n e s for Heliothis population analysis a n d synthesis of the p h e r o m o n e s of Helio• suppression does not look very promising at this this spp in recent years, but we must now deter• time. Attempts to disrupt mating using the phero• mine whether the synthetic p h e r o m o n e mixtures mones have not yet produced very encouraging are going to be of practical value in Heliothis m a n • results. T h e prospects for the utility of m a s s trap• agement. Considerable numbers of male moths ping appear to be even more discouraging, partly c a n be caught in a variety of traps baited with b e c a u s e of the considerable mobility of the moths, various substrates that allow the evaporation of the but also because some studies have indicated synthetic pheromones. large n u m b e r s of male moths are trapped only T h e most probable practical use of the synthetic several days after peak moth e m e r g e n c e and peak p h e r o m o n e s lies in monitoring populations. Forthis mating have occurred. Additionally, even the most there is first a need to standardize trap design, efficient traps apparently c a t c h less than 5 0 % of p h e r o m o n e dosage a n d release rates from the the males attracted to within a meter of the trap. chosen substrate, and siting of the traps. Catches However, s o m e s u c c e s s in population suppression in these traps have to be c o m p a r e d with other using m a s s trapping has been reported from Israel. measures of Heliothis populations, including light T h e identification of other attractants w a s briefly traps a n d actual counts of Heliothis eggs a n d lar• discussed. S o m e c h e m i c a l s are k n o w n to attract vae, on the host plants in the area of the traps. both male a n d female Heliothis moths, but the Preliminary studies have already indicated that the attraction is weak, and catches in traps baited with c a t c h e s in p h e r o m o n e traps do not correlate very these substances are low. However, the e n o r m o u s well with light-trap c a t c h e s and field c o u n t s of the payoff that would result from the identification of a pest in all circumstances. However, data from c h e m i c a l mixture that is very attractive to the p h e r o m o n e traps have already been s h o w n to be of female moths should e n s o u r a g e further research.

4 0 9 Sterile Hybrids Session 7: Integration of Management T h e e n c o u r a g i n g results obtained on St. Croix Island, using the H, virescens x H. subflexa hybrid Discussion Leader: M.J. Lukefahr for population suppression, stimulated discussion on the future of such initiatives. This test should T h e current status of k n o w l e d g e on various m a n • now be repeated over a larger area. Additionally, a g e m e n t c o m p o n e n t s w a s d i s c u s s e d with particu• the possibility of producing similar sterile hybrids lar reference to their utility in an integrated using other s p e c i e s a n d H. zea a n d H. armigera as pest-management system. It became evident that parents s h o u l d be investigated. Biosystematic a n d m u c h m o r e information w a s n e e d e d o n e c o n o m i c crossing studies might best be c o n d u c t e d in labor• thresholds, crop loss estimates, scouting methods, atories in countries s u c h as UK, w h e r e Heliothis is insect behavior, population dynamics, and the dia• unlikely to become a pest. Backcrossed progeny p a u s e / a e s t i v a t i o n of Heliothis on a regional basis. f r o m promising s p e c i e s combinations c a n t h e n b e In the c a s e of e c o n o m i c threshold levels, differen• transferred to the target areas for behavioral stu• c e s in c o s t s a n d e c o n o m i c returns f r o m different dies a n d eventual evaluation. crops a n d areas will ensure that these have to be r e s e a r c h e d a n d calculated for e a c h c r o p on a Recommendations national or even area basis. From the available information on several m a n • 1. Monitoring Heliothis a b u n d a n c e w i t h agement components, including host-plant resist• pheromone-baited traps appears to be a most a n c e a n d the use of microbials, it woul d appear promising area for r e s e a r c h in developing c o u n • that, in most areas, these are still a long way from tries. T r a p s a n d baits should be standardized as far implementation in farmers' fields. as possible, at least on a regional basis. Trap-catch Development of crop loss assessment metho• data should be related to information from other dology a n d studies of cultural practices s u c h as monitoring d e v i c e s s u c h as light traps, to estimates c r o p rotations a n d c l o s e d seasons, of s o u r c e s of of n u m b e r s of e g g s a n d larvae in the crop, c r o p pest populations, and of the use of selective pesti• damage, crop phenology, and weather. The devel• cides for the conservation of biocontrol agents may opment of a central repository for such information all p r o d u c e worthwhile data that c o u l d have an should be e n c o u r a g e d a n d analysis of results impact in the near future on the m a n a g e m e n t of should be undertaken on a collaborative basis with Heliothis spp, particularly in the semi-arid areas of organizations having expertise in this area, e.g. the developing countries. Centre for O v e r s e a s Pest R e s e a r c h (UK) a n d the Although we are still a long w a y from being able m o d e l i n g units of the U n i t e d States Department of to formulate integrated pest-management strate• Agriculture. gies that are a n y w h e r e near ideal for most farmers 2. T h e r e s e a r c h on mating disruption of Heliothis is a n d areas, we have certainly progressed b e y o n d still at a relatively early stage in developed coun• the stage where the only advice that we c a n give tries, a n d it is r e c o m m e n d e d that organizations in the farmer is to spray pesticides w h e n e v e r he sees developing countries s h o u l d r e m a i n informed of Heliothis e g g s or larvae in his crop. T h e r e is already this work without initiating programs of their o w n — an a b u n d a n c e of e v i d e n c e to show that total at least until the merits of mating disruption of Heli• reliance upon pesticides for Heliothis management othis are obvious. is d o o m e d to failure, with c o n s e q u e n t major prob• 3. Mass trapping does not appear, at present, to be lems. It is obvious that there is unlikely to be a a feasible control strategy for Heliothis spp. Any p a n a c e a for Heliothis m a n a g e m e n t in the near n e w initiatives in this area should be carefully future. M a n a g e m e n t strategies are likely to remain a s s e s s e d . relatively specific to a site, or at least a region. 4. It is recommended that a central location, per• haps in the UK, be established for biosystematic Recommendations studies of Heliothis spp. T h i s initiative should be e x t e n d e d to work on the development of a p p r o p • 1. E c o n o m i c injury levels for the major crops riate sterile Heliothis hybrids w h e n it is c o n s i d e r e d should be established. that sufficient progress has b e e n m a d e in the pilot 2. Methods of monitoring populations should be programs s u c h as those in the USA. developed.

4 1 0 3. The use of pheromones should be studied, par• ticularly in relation to monitoring populations. Ad d i • tional studies of the long-range movement of Heliothis spp moths are required in most regions. 4. Many potential elements of Heliothis m a n a g e • ment were presented at this workshop, but most are not yet sufficiently advanced to be of practica• ble use in any generally applicable pest- management strategy. 5. Additional studies need to be made on closed seasons, sowing dates, crop rotations, and other cultural practices that are components of pest management systems.

411

Appendix 1 Participants International Workshop on Heliothis Management

Rear row (standing): H. Rembold, D.S. Hackett. A.G.L. Wilson, G.H.L. Rothschild, T.J. Lawson, A. Kohli, R.J.V. Joyce, D.J. Rogers, P.D. Lingren, Galal El Din Hamid Osman, D.J. Greathead, J.A. Gledhill, W.V. Campbell. Second row (standing): P.H. Twine, K.S. Kushwaha, A.K. Karel, A.N. Balla, HP. Saxena, K.S. Chhabra, Zile Singh, T.S. Thontadarya, M. Jacobson, D.J. McKinley, E.G. King, A.C. Bartlett, N. Ramakrishnan, J.C. Davies. Third row (sitting): K.D. Paharia, M.J. Haggis, Sudha Nagarkatti, R.C. Patel, S. Jayaraj, J.S. Kanwar (Director of Research, ICRISAT), L.D. Swindale (Director General, ICRISAT), J.R. McLaughlin, M.R. Bell, A.C. Waiss, Jr., B.R. Wiseman, A.N. Sparks, B. Nyambo. Front row (sitting): S. Sithanantham, W. Reed, E. Winter, C.S. Pawar, A.B. Mohammed, P.W. Amin, H.C. Sharma, S.S. Lateef. Participants

P.W. A m i n J.A. Gledhill Groundnut Entomologist Head, Cotton Research Institute ICRISAT Center Private Bag 765 Patancheru,A.P. 502324, India. Gatooma, Zimbabwe

A . N . Balla D.J. Greathead Agricultural Research Corporation Assistant Director Gezira Research Station Commonwealth Institute of Entomology Section Biological Control Wad Medani, Sudan Imperial College, Silwood Park Ascot, Berks SL5 7PY, UK A.C. Bartlett Research Geneticist D.S. Hackett USDA Western Cotton Research Laboratory Wizara Ya Kilimo 4135 East Broadway Rd Kituo Cha Utafiti Wa Kilimo Phoenix, AZ 85040, USA llonga S.L. Pekee, Kilosa, Tanzania M.R. Bell Research Entomologist M.J. Haggis USDA Western Cotton Research Laboratory Centre for Overseas Pest Research 4135 East Broadway Rd College House Phoenix, AZ 85040, USA Wrights Lane, London W8 5SJ, UK

W.V. Campbell G. Hariri Professor, Dept. of Entomology ICARDA North Carolina State University P.O. Box 5466 Box 5 2 1 5 Aleppo, Syria Raleigh, NC 27650, USA A.W. Hartstack, Jr. K.S. Chhabra Agricultural Engineer Senior Entomologist and USDA Pest Control Equipment and Principal Investigator Methods Research Unit AICPIP-ICAR Room 231 Agricultural Engineering Building IARI, Regional Station Texas A & M University Kanpur 208 024, India College Station, TX 77843, USA

J.C. Davies M . J a c o b s o n Director, International Cooperation Chief, Biologically Active ICRISAT Center Natural Products Laboratory Patancheru.A.P. 502324, India Agri Environmental Quality Institute Beltsville Agricultural Research Center Galal El Din Hamid Osman Beltsville, MD 20705, USA Chief Entomologist Agricultural Research Corporation A.P. Jaiswal Gezira Research Station Scientist S-3 Entomologist Wad Medani, Sudan Central Institute for Cotton

4 1 5 Research (ICAR) P.D. Lingren 95, Pushp Kunj, Canal Road Research Entomologist, USDA New Ramdaspeth, Nagpur 440 010, India Western Cotton Research Laboratory 4135 East Broadway Road S. J a y a r a j Phoenix, AZ 85040, USA Director of Research (Agriculture) Tamil Nadu Agricultural University M.J. Lukefahr Coimbatore 641 003, Tamil Nadu, India Research Entomologist International Institute of R.J.V. Joyce Tropical Agriculture 29 Kimbolton Road Oyo Road, PMB 5320 Bedford MK 40 2PB, UK Ibadan, Nigeria

A.K. Karel N o w at: Senior Lecturer in Entomology Centro Nacional de University of Dar-Es-Salaam Pesquisa da Algodao P.O. Box 6 4 3 Caixa Postal, 174 Morogoro, Tanzania 58100 Campina Grande Paraiba, Brazil E.G. K i n g Laboratory Chief D.J. McKinley Southern Field Crop Centre for Overseas Pest Research Insect Management Laboratory Division of Chemical Control Delta States Research Center Porton Down, Salisbury P.O. Box 2 2 5 Wiltshire SP4 0JQ, UK Stoneville, Miss 38776, USA

J.R. McLaughlin A. Kohli Research Entomologist Regional Entomologist USDA, Insect Ecology Far East and Pacific Region 1700 SW 23rd Drive, P.O. Box 14565 Imperial Chemical Industries Ltd. Gainesville, Fla 32604, USA Fernhurst, Haslemere, Surrey GU27 3JE, UK

K.S. Kushwaha J.A. M i h m Professor of Eminence Entomologist, CIMMYT Department of Entomology Londres 40 Mexico-6, D.F. Rajasthan College of Agriculture Apdo Postal 6-641 University of Udaipur, Udaipur 313 001, India M e x i c o

S.S. Lateef A.B. Mohammed Pulse Entomologist Groundnut Entomologist ICRISAT Center ICRISAT Center Patancheru, A.P. 502 324, India Patancheru, A.P. 502 324, India

T.J. Lawson Sudha Nagarkatti CIBA-GEIGY Research Unit Indian Institute of Horticultural Research Agricultural Aviation Research Unit 142-111 Main Road Cranfield Institute of Technology Ganganahally Layout, Bangalore 560 006, India Cranfield, Bedford MK43 OAL, UK B. N y a m b o K. Leuschner Entomologist Principal Cereal Entomologist Ukirigiru Research Institute ICRISAT Center P.O. B o x 1433 Patancheru, A.P. 502 324, India Mwanza, Tanzania

4 1 6 I.W.B. N y e Department of Primary Industries British Museum (Natural History) P.O. Box 23 Cromwell Road Kingaroy, Old 4610, Australia Londo n SW7 5BD, UK G.H.L. Rothschild K.D. Paharia Senior Principal Research Scientist Plant Protection Advisor C S l R O Division of Entomology to the G o v e r n m e n t of India P.O. Box 1700 Directorate of Plant Protection Canberra City, A C T 2 6 0 1 , Australia Quarantine a n d Storage 4 0 9 B Wing, Shastri B h a v a n H.P. S a x e n a N e w Delhi 110 0 0 1 , India Sr. Entomologist Indian Agricultural Research Institute R.C. Patel N e w Delhi 110 012, India Program Executive (Res) Gujarat Agricultural University H.C. S h a r m a A n a n d 388 100, India. Sorghum Entomologist ICRISAT Center C.S. P a w a r Patancheru, A.P. 502 324, India Pulse Entomologist ICRISAT Center S. S i t h a n a n t h a m Patancheru, A.P. 502 324, India Pulse Entomologist ICRISAT Center F.I. Proshold Patancheru, A.P. 502 324, India Location Leader, USDA Federal Experiment Station A . N . Sparks P.O. Box H, Kingshill Laboratory Director St. Croix, U.S. Virgin Islands 00850, USA USDA Southern Grain Insects Research Laboratory N. R a m a k r i s h n a n Tifton, GA 31793, USA National Fellow Division of Entomology S . L . T a n e j a Indian Agricultural Research Institute Cereal Entomologist N e w Delhi 110 012, India ICRISAT Center Patancheru, A.P. 502 324, India J.R. Raulston Research Entomologist T . S . T h o n t a d a r y a USDA Cotton Insects Research Professor a n d H e a d P.O. Box 1033 Department of Entomology Brownsville, TX 78520, USA Agricultural College, Hebbal

W . R e e d Bangalore 5 6 0 024, India Principal Pulse Entomologist ICRISAT Center P.H. T w i n e Patancheru, A.P. 502 324, India Senior Entomologist Department of Primary Industries H . R e m b o l d P.O. Box 102 H e a d , Insect Biochemistry T o o w o o m b a 4350, Old, Australia Max-Planck Institute for Biochemistry 8 0 3 3 Martinsried bei M u n i c h A . C . Waiss, Jr. West G e r m a n y Research Leader USDA Plant Protection Phytochemistry D.J. R o g e r s R e s e a r c h Unit Entomologist Western Regional Research Center

4 1 7 800 Buchanan St Berkeley, CA 94710, USA

A.G.L. Wilson Senior Research Scientist CSIRO Division of Plant Industry Cotton Research Unit P.O. Box 59, Narrabri, NSW 2390, Australia

E. W i n t e r Max-Planck Institute for Biochemistry 8033 Martinsried bei Munich West Germany

B.R. Wiseman Research Entomologist USDA Southern Grain Insects Research Laboratory Tifton, GA 31793, USA

Zile S i n g h Professor a n d H e a d Department of Entomology Haryana Agricultural University Hissar 125 004, India

4 1 8 RA-0046 ICRISAT

International Crops Research Institute for the Semi- Arid Tropics

ICRISAT Patancheru P.O.

Andhra Pradesh 502 324, India