Use of Bacillus thuringiensis in integrated control, especially on cotton pests

ELSEVIER Agriculture, Ecosystems and Environment 49 (1994) 77-83

Agriculture Ecosystems & Environment

Use of Bacillus thuringiensis in integrated control, especially on cotton pests

Neil W. Forres ter

NSW Agriculture, Agricultural Research Station, Myall Vale via Narrabri, N.S. IV.. 2390, Australia

Abstract

The resurgence of interest in Bacillus thuringiesis (Bt) in the Australian cotton industry is discussed principally in relation to increasing resistance problems and heightened environmentalism. The use of Bt in the cotton industry has been strategically targeted to two key areas: early season mixtures with below recommended rates of endosulfan (to reduce environmental contamination) and mid-season mixtures with pyrethroids (for resistance management). The current relatively high price of Bt (compared with conventional synthetic alternatives) is seen as a major constraint to the wider adoption of effective rates of Bt. Two incentive schemes, aimed at encouraging greater use of Bt, lowering the cost through economies of scale and engendering interest in a local fermentation facility, are discussed. The potential market for Bt in Australian cotton is assessed conservatively at 2 and possibly up to 5 million I annually. The resistance risk of this extensive usage is discussed, particularly in relation to its potential interaction with the possible misuse of transgenic cotton expressing Bt toxin (s). The requirements for the design of a 'perfect' Bt for cotton are discussed.

1. Introduction

Bacillus thuringiensis (Bt) has been used for heliothis control on field crops in Australia for some years now, with mixed success. Successful control using Bt alone has not been widely achieved probably because of a combination of factors: lower quality of early formulations; less than optimal application techniques leading to poor contact with larvae on crops with protected feeding sites (especially cotton); improper tar- geting of larger sized larvae; use of low inade- quate rates in an endeavour to reduce cost and probably most importantly, excellent control with cheaper alternative synthetic insecticides. Arguably the most successful past use of Bt was as a mixture with chlordimeform in cotton. The

Elsevier Science B.V. SSDI0167-8809(93)02014-5

Table 1 Volume of Bacillus thuringiensis used in the Australian cotton industry before and after the withdrawal of chlordimeform in November 1986

Year Chlordimeform Annufl useage available (1)

Pre-1986 Yes 20000-30000 1986-1990 No 8000-12000 1990/1991 No ~ 100000 1991/1992 No ~ 180000

Source: K. Watts, Cotton Grower Services Pry. Ltd., Wee Waa, N.S.W. and N.W. Forrester (unpublished data, 1992).

fumigant action, ovicidal activity and larval be- haviour modifying properties of chlordimeform seemed to complement the stomach action of Bt

78 N.W. Forrester /Agriculture, Ecosystems and Environment 49 (1994) 77-83

on larvae. However, after the withdrawal of chlordimeform in 1986, Bt use declined to low levels because of the lack of a suitable alternative mixing partner (Table 1 ).

2. Current situation

However, in the past few years, two factors have combined to stimulate a resurgence of interest in Bt in cotton; increasing pyrethroid resistance problems in Helicoverpa armigera (Forrester, 1989, 1991a)and increased public concern on environmental issues (Short, 1989; Murphy, 1990; Whyte and Conlon, 1990; Hou- lahan, 1991; Jeffreys, 1991; Baker, 1991; Black, 1991; Watt, 1991 ). The introduction of an insecticide resistance management (IRM) strategy in Australia in 1983/1984 (Forrester, 1990) de- creased the use of pyrethroids in the cotton industry with a concomitant increase in the use of alternative compounds, particularly endosulfan and organophosphates. These compounds have particular environmental drawbacks such as acute fish toxicity (endosulfan) (Guerin and Kennedy, 1991 ) and off-target drift of offensive mercaptan odours (e.g. profenofos, sulprofos) (Brock, 1989). The use of Bt in the cotton industry is now strategically targeted to two key areas: early season mixtures with below recommended rates of endosulfan (and to a lesser ex- tent thiodicarb) and mid-season mixtures with low rates of pyrethroids. The aims of these two uses are distinct. The first aims to reduce the pesticide load on the environment by reducing the normal endosulfan rate (by one-half to one- third) and 'topping up' with a biological insecticide. This can only serve to improve the environmental image of the cotton industry, help retain the registration of endosulfan and promote the sustainability of the cotton production system. The second aim of Bt (with pyrethroids) is to provide a 'safety net' for the pyrethroids by kill- ing resistant larvae which may survive the pyrethroid component of the mixture. This complementary additive activity of Bt with pyrethroids is also very important for the preservation of the efficacy of the pyrethroid synergist piperonyl bu-

toxide (Pbo). Because of the resistance risk, Pbo is recommended to be used with only one of the three pyrethroids recommended per season. Hence Bt is recommended as a second de facto pyrethroid synergist to rotate with Pbo (Shaw, 1992). The main benefit of the Bt/pyrethroid mixture is improved IRM which is also a side benefit of the Bt/endosulfan mixture when endosulfan-resistant H. armigera are present, particularly later in the season and in the more northerly growing areas. Other factors also con- tributed to the recent increase in use of Bt in cotton.

One factor was the development by Abbott Laboratories of an improved formulation of Bt (DiPel ES) which allowed greater flexibility of use. This higher strength emulsifiable suspen- sion proved to be equally compatible with both aqueous emulsifiable concentrates (ECs) and the oil-based ultra low volume (ULV) formulations preferred by the majority of the cotton industry. The general improvement in application techniques in the Australian cotton industry over the past decade (Harden, 1987; Shaw, 1987; Sutton, 1987; Weatherstone, 1988; Harden and Woods, 1989; Bodnaruk, 1990) has also assisted greatly in delivering Bt to the target site. This, of course, is of critical importance for stomach poisons such as Bt (Cameron, 1990) and poor application was no doubt one of the factors limiting the successful use of Bt in the past.

Bt fits well into the current integrated pest management (IPM) programme for cotton (Forrester and Fitt, 1992). 'Soft' insecticides, which have the least detrimental impact on ben- eficial insects, are used early in the season (e.g. endosulfan, the carbamate thiodicarb and, hope- fully in the future, the benzoylphenylurea chitin inhibitor chlorfluazuron). Bt fits well into this early use niche and is considered to be a direct competitor with the similar stomach-action insecticides chlorfluazuron and thiodicarb. How- ever, Bt may have some advantage over these insecticides in relation to its better compatibility with the environment (currently the effect of benzoylphenylurea chitin inhibitors on aquatic invertebrates is in question) and its ability not to induce secondary mite problems (high rates

N. W. Forrester /Agriculture, Ecosystems and Environment 49 (1994) 77-83 79

of thiodicarb may possibly cause flaring of mites). However, the lack of contact action puts Bt at a disadvantage in comparison with endosulfan, particularly in cotton where feeding sites are protected from sprays. Intuitively, a mixture of Bt and reduced rates of endosulfan should be a complementary combination for optimal management of pests and minimal impact on the environment and indeed, this is the mixture which has been accepted in commercial practice in cotton. The role of Bt in integrated control in other field crops will probably follow along the same lines as for cotton. That is, mixtures of contact insecticides (e.g. endosulfan, pyrethroids) with Bt will be used in crops with protected feeding sites (e.g. sweetcorn, summer grain legumes) and

Table 2 Recommendations ~ for the use of Bt in Australian cotton

Rate DiPel ES Critical comments

1-21/ha-

1-2 l / h a - 1 + thiodicarb ( 175-350 g a.i. ha - I )

1-2 l / ha - 1 + endosulfan (360-480 g a.i. ha - I )

Apply DiPel ES alone only in pre- squaring cotton. Use the 11 rate under egg pressures of up to one egg per terminal and the 21 rate under egg pressures of up to two eggs per terminal Use the lower rate of DiPel ES and thiodicarb where egg pressure is less than three eggs per terminal. Use the higher rate of DiPel ES if hatching larvae are present and increase the thiodicarb rate for larger larvae up to 8 mm Use the lower rate of DiPel ES and endosulfan where H. punctigera is the dominant species, egg pressure is less than two eggs per terminal and larvae are smaller than 8 ram. Use the higher rates of DiPel ES where H. armigera predominates. Use higher rates of endosulfan under higher egg pressures and /o r where larger larvae are present

t Recommendations for the use of Bt in Australian cotton, ex- tracted from the current Abbott registration label for DiPel ES ( 17.6 billion IU of potency 1- ~ Bacillus thuringiensis Ber- liner var. kurstaki) for the control ofHeliothis spp. on cotton in New South Wales and Queensland, Australia. Note: pyr- e throid/Bt mixes are not currently registered in Australia. They will be used commercially for the first time in the 1991 / 1992 season, subject to a pending Pesticide Order.

Bt may be successfully used alone in crops with relatively easily accessible larvae (e.g. soya beans, lucerne, sunflowers, sorghum, winter grain legumes, cabbages). Bt could be particularly useful in sunflowers and lucerne where heliothis control may be necessary when pollinating bees are active at flowering. However, the generally larger size of larvae which need to be controlled in these crops (because of less frequent checking inter- vals) could well be a factor limiting wider adoption of Bt in these crops (Bryant, 1994)

As discussed previously, Bt use in cotton, at least initially, will be at lower rates in mixtures with synthetic insecticides such as endosulfan and pyrethroids. Bt alone can effectively control heliothis in cotton but the rates needed (two to three times those currently used) would be eco- nomically prohibitive (see following section). So for the time being, Bt use in Australian cotton will remain principally as a mixture component with conventional insecticides. There is a niche for the use of Bt alone in young pre-squaring cotton in low pest pressure situations (Table 2 ), but this is a relatively minor use.

3. Future situation

There is no doubt that there are now strong incentives for the increased use of Bt in Australian cotton. However, the major factor acting against wider adoption is the high cost of Bt, relative to the synthetic alternatives. Pyrethroids and endosulfan for heliothis control currently sell for around A$18 ha -~ and the organophosphates (e.g. profenofos) and carbamates (e.g. thiodicarb) are about twice this cost. Bt is significantly more costly than the conventional alternatives. For example, Dipel ES ( 17.6 billion IU 1- t ) cost A$17.501 -~ retail in 1990/1991 (A$14.801 - t in the 1991 / 1992 season). Although registered for use in mixtures with endosulfan down to 1.0 1 DiPel ES ha-l , most use is expected to be at a minimum of 1.5 1 DiPel ES ha-~ and preferably up to 2.0 1 DiPel ES ha -1 (see Table 2). Table 3 gives the cost of the various Dipel/endosulfan mixture combinations. It is clear that as long as

80 N. W. Forrester /Agriculture, Ecosystems and Environment 49 (1994) 77-83

Table 3 Cost of Bt/endosulfan mixtures (A$ ha- t, 1991 prices)

Rate DiPel ES (l /ha- l ) + endosulfan (g ha- ~ )

Cost of Bt (AS 1 -m )

17.50 15 10 6

Full rate endosulfan alone (720) 18.00 18.00 18.00 18.00 DiPel 1.0 + 360 endo 26.50 24.00 19.00 15.00 DiPel 1.0+480 endo 29.50 27.00 22.00 18.00 DiPel 1.5+360 endo 35.25 31.50 24.00 18.00 DiPel 1.5+480 endo 38.25 34.50 27.00 21.00 DiPel 2.0 + 360 endo 44.00 39.00 29.00 21.00 DiPel 2.0 + 480 endo 47.00 42.00 32.00 24.00

A $1 is approximately equal to US$0.71.

the cost of Bt remains high (e.g. more than A$15 1-1 ) and the cost of endosulfan remains low, growers will be tempted to adopt the lower, marginally effective rates of Bt. The preferred rates of Bt (equivalent of 1.5-2.01 ha- ~ DiPel ES) do not become cost attractive to growers until the Bt price drops to around A$10 1-1. Even then, growers will be expected to pay 33-78% more for the endosulfan/Bt mixture than for endosulfan alone at full rate.

The high price of Bt has also proved to be a problem in other countries. For example, in the USA the difficulty of getting increased Bt use on potatoes for Colorado potato beetle control is that it is at least 50% more expensive than the alternatives (R. Roush, personal communication, 1991 ). As the volumes of Bt used increase, economies of scale should begin to operate. In Aus- tralia the problem is exacerbated by the absence of local production: at present all Bt must be im- ported which adds significantly to the cost. A critical volume of sales must be reached ( 106 1 annually?) before a local production facility be- comes an economic proposition. Currently, manufacturers are unwilling or unable to reduce the cost of Bt to the grower until the volume sold goes up. The volume sold will not increase until the price comes down. This nexus must be breached to avoid the retrograde step of growers cutting rates of Bt to make it an economic proposition for commercial use. The adoption of marginally effective rates will lead to erratic performance and a reputation for inconsistency that

will be difficult to rectify. Growers are willing to pay more for the long-term IRM and environmental benefits of Bt, but only up to a certain point. They are also aware that higher prices mean greater incentives to the Bt manufacturers for the future development of more virulent strains, better formulations and delivery sys- tems, etc. However, immediate economic sur- vival and the containment of production costs are also of major concern to the unsubsidised Aus- tralian cotton industry in a highly competitive and price-sensitive cotton export market. The price of Bt needs to fall to around A$10-12 1-1 to encourage the greater use of Bt in the Austra- lian cotton industry. Two separate schemes are suggested to help reduce the retail price of Bt.

3.1. Tax relief for the use of biological insecticides

Tax deduction allowances already exist in Australia to encourage certain desirable activi- ties (e.g. 150% deduction for company research and development expenditure). A similar scheme could be designed to encourage the greater use of Bt. Thus, a scheme allowing say, 200% deduction for expenditure on biological alternatives to conventional synthetic alternatives, would be a very strong incentive for growers to increase their use of Bt. To make this proposal more attractive to the taxation authorities, a 'sunset' clause could be incorporated allowing for a 25% reduction in the allowance each year, until it cuts out after 5 years. This proposal spreads the cost over the en-

N. W.. Forrester /Agriculture, Ecosystems and Environment 49 (I 994) 77-83 81

tire community and could be viewed as the cost of investing in a better environment. It would also serve to create an image overseas of 'envi- ronmentally sound' Australian rural produce, which can only be an advantage in today's highly competitive export markets. Such a proposal would most probably be politically neutral and should draw support from all political parties and a diverse range of consumer and environmental interest groups.

3.2. Temporary levy on conventional synthetic insecticides

A temporary levy could be imposed on the sales of the synthetic insecticide component in the mixtures currently used. A 5% levy on endosulfan (A$0.301-1 ) and a 1.7% levy on pyrethroids (AS0.10 1-1 ) would raise approximately AS1 million annually which could then be redistri- buted back to the growers who used Bt. One Bt spray per cotton area (250 000 ha) at 1.5 1 ha - 1, would result in a rebate to growers of around A$3 1-1 of Bt used. This levy would probably only need to be in place for two to three seasons to provide sufficient incentive to increase Bt use to two or three sprays per cotton area. This should be sufficiently high to trigger a price reduction through economies of scale. This proposal is self- funding in that it spreads the cost over the growers and then redistributes it back to the innova- tors within the farming community. One of the problems with this proposal is that the more successful it is, the less the rebate to the Bt user (as Bt use goes up, endosulfan use will go down, the revenue raised will in turn decline and will have to be distributed over a larger volume of Bt used). Also, the administration of the levy could be complex and many growers would be very cau- tious of the precedent set in imposing a levy on one of their production inputs.

Both the above proposals aim to break the price/volume nexus discussed earlier, differing mainly in the apportioning of the cost subsidy. If adopted, these proposals should result in an increased use of Bt which would then establish Bt as a reliable component of the Australian cotton insect control market. This in turn might en-

courage overseas Bt manufacturers to establish a joint venture local fermentation facility. This should further lower the price of Bt and encourage its wider adoption in Australian agriculture.

4. Potential market and resistance risk

If the problem of the relatively high cost of Bt is solved, then the potential for Bt in the Austra- lian cotton market is quite considerable. If one assumes that Bt/conventional insecticide mixtures will be adopted initially, then the market is potentially five Bt/endosulfan or Bt/thiodicarb sprays in the early Stage 1 period (Forrester, 1990) and a single Bt/pyrethroid spray during the Stage 2 pyrethroid window. Based on a cotton area of 250 000-300 000 ha and a preferred mixture rate of 1.5 1 ha-1, then the market for Bt could be 2.3× 10 6 to 2.7× 10 6 1. I fB t alone (at 3-41 ha - 1 ) was to completely supplant endosulfan, then the potential market could rise even further to around 5 × 1061.

At these levels of use, the question is whether resistance will develop to Bt. It seems unlikely. Most of the Bt will be used in the early Stage 1 period where the predominant pest is Helicov- erpa punctigera rather than the recidivist resistance-prone H. armigera. Because of its different ecology, H. punctigera has not developed resistance to any conventional synthetic insecticide and is unlikely to ever do so (Forrester et al., 1993 ), so the resistance risk with the biological insecticide Bt is also likely to be low. In Stage 2 there will be only one spray in mixture with a pyrethroid and no Bt will be recommended in the H. armigera dominant late season Stage 3 period, where quite effective alternatives such as thiodicarb, chlorfluazuron and profenofos are available. The extensive use of Bt against H. armigera in other field crops such as chickpeas and summer grain legumes, oilseeds and coarse grains, could pose a potential problem and should be closely watched, although satisfactory cost-effective alternatives (especially thiodicarb) do exist for these crops. Caution will also be needed in the more northerly cotton growing areas such as central Queensland, where H. armigera tends

82 N. W. Forrester /Agriculture, Ecosystems and Environment 49 (1994) 77-83

to be more abundant earlier than in the south. If the proposed guidelines are followed, there are unlikely to be problems and the greatest threat of resistance development to Bt will remain the misuse of the transgenic cotton technology (see Llewellyn, 1994). The extensive and unres- trained sowing of transgenic cotton expressing only one (or even two) Bt protein gene(s) throughout the life of the plant, could very quickly result in the development of resistance to Bt. This would then prejudice the whole development of the conventionally produced/applied Bt fermentation product. This potential problem must be addressed in the very near future.

5. The perfect Bt for cotton

Cotton is a very difficult crop to protect as it is subject to rapid growth dilution, has well protected feeding sites and a wide range of primary and inducible secondary pests (Forrester, 1991b). Ideally, a Bt for use in cotton should have the following properties:

( 1 ) high virulence for the local heliothis species ( H. punctigera and H. armigera ) ;

(2) suitable formulations for: (i) aerial mixes (need to be compatible with both water based emulsifiable concentrate and oil-based ultra low volume formulations); (ii) aerial alone (should be suitable for use down to a total volume of 3 1 ha - ~ ); (iii) ground application ( should be water- dispersible granules or soluble powders in water- soluble packaging for the completely 'environ- mentally friendly' Bt);

(3) availability of exotoxins for optional ad- dition for contact activity against mirids and translaminar activity against mites. Preferably, the exotoxin should also be non-toxic to the important thrip predators of mites.

(4) Increased residual activity from the current 3-4 days to that of a pyrethroid (say 5-6 days, as limited by growth dilution).

( 5 ) Low cost to promote use at adequately high rates for consistent and reliable control (say A$6-81- ~ ).

Some of these requirements may never be met but at least the goals are clearly defined.

6. Conclusion

Bt has had a chequered past in cotton in Aus- tralia. The recent renaissance of Bt in the Austra- lian cotton industry can be attributed to the al- lied problems of resistance development to conventional chemicals and revived concerns for the environment. This resurgence (in interest in Bt) could be put at risk from the relatively high price of Bt, inducing the use of marginally effective low rates. This will lead to claims of inconsistency and unreliability of performance which were common complaints against Bt in the past. This problem must be resolved so that growers have access to affordable and cost-effective rates of Bt.

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Use of Bacillus thuringiensis in integrated control, especially on cotton pests