The efficacy of alternative compounds to organophosphorus pesticides for the control of storage mite pests

SUMMARY
Mites are very common pests of stored cereals and oilseed in the U. K. As well as the damage they cause through feeding, heavy infestations can taint grain making it unpalatable to livestock and unsuitable for milling. They also present a serious health risk through the development of allergies and have been implicated in the transmission of micro-organisms. In the U. K., stored grain protection in the past has relied heavily on bulk admixture with contact pesticides. Today only organophosphorus (OP) pesticides are approved for this use. None of these pesticides are particularly effective against field strains of mites and resistant populations have been detected. As well as concerns regarding the development of resistant pests, the costs and consumer resistance to toxic chemicals in food, have led to increasing pressures for a reduction in pesticide use. Cooling and drying effectively prevent infestations developing in the bulk, but the surface layers remain vulnerable to infestation and may require a pesticide treatment.

The aim of this project was to identify potential alternatives to OPs and to investigate their efficacy against storage mite pests. A literature review identified potential candidates and from this, 21 compounds were selected for initial screening. Selection was based on efficacy against other acarine pests and the availability of commercial formulations. The compounds included 4 or 5 representatives of diatomaceous earths (DEs), insect growth regulators (IGR), novel compounds, pyrethroids, biological control agents and botanicals. Efficacy was assessed, admixing each compound with wheat, against mixed stages of susceptible strains of Acarus siro L., Lepidoglyphus destructor (Schrank) and Tyrophagus putrescentiae (Schrank) at 15oC and 75% relative humidity. Population inhibition was assessed after periods long enough to include the passing of at least 2 generations under control conditions. The most effective compounds from each group were found to be the DE 'Protect-it', the IGR, flufenoxuron, the novel compounds, sodium polyborate and benzyl benzoate, the pyrethroid, bifenthrin and the botanical, azadirachtin.

These six compounds were then further assessed against OP susceptible and resistant strains of mites and insects (A. siro, L. destructor, T. putrescentiae, Sitophilus granarius (L.), Oryzaephilus surinamensis (L.) and Rhyzopertha dominica (Fabricius). Four doses of each compound were applied to wheat which was stored at 10oC or 25oC at 75% r.h. and then sampled 1 day, 4 weeks and 12 weeks after treatment. Efficacy was evaluated by the effect on adult beetle mortality and on the ability of the compounds to inhibit development of the insect and mite populations at the two temperatures. The results indicated the range of tolerances of the different pest species and strains to the different compounds, with Sitophilus granarius, appearing the most tolerant species. In general, lower doses of the pesticides were required to inhibit the mite populations when exposed at 10oC compared to 25oC and adult insect mortality was higher at 25oC than at 10oC. The chitin synthesis inhibitor, flufenoxuron, and the plant extract, azadirachtin, were considered to be worthy of further investigation.

In the next stage of testing, batches of wheat were treated with flufenoxuron and azadirachtin, put into small bins, infested with mixed populations of mites and insects (A. siro, L. destructor, S. granarius and O. surinamensis) and stored at 15oC and 80% rh for 26 weeks. After a 2-week assessment, efficacy was evaluated at 4 weekly intervals by the ability of the compounds to inhibit the development and survival of the pest species. No A. siro or L. destructor were detected in the samples treated with flufenoxuron at or after 6 and 10 weeks respectively. In the azadirachtin-treated samples no mites were detected from week 2 up to week 26 when A. siro were found in one of the bins. However, no L. destructor were detected in any of the untreated samples after week 14 which may have been due to competition from the faster breeding A. siro. Adult beetles were caught in the traps throughout the experiment with lower numbers of O. surinamensis trapped than S. granarius. The treatments reduced the numbers of S. granarius by approximately 75 %.

In addition to wheat, it was also considered important to assess effectiveness on oilseed rape, as mites are common pests on this commodity, and from earlier this year, phosphine is the only pesticide approved for use. The efficacy of flufenoxuron, azadirachtin and the diatomaceous earth 'Protect-it' were assessed, when admixed with oilseed rape, against susceptible strains of A. siro, L. destructor and T. putrescentiae. Population inhibition was evaluated in experimental conditions of 15oC and 80% rh after the passing of at least one generation. 'Protect-it' appeared the most effective treatment against all the mite species with a dose of 3 g kg -1 inhibiting the populations by > 96 %. Flufenoxuron was highly effective at all doses against L. destructor, with azadirachtin appearing the least effective against all the species at the doses assessed.

Previous MAFF-funded research had found diatomaceous earths to be effective against insects and mites. However, information was lacking as to their efficacy against an existing mite infestation. Therefore in the final phase of this project the diatomaceous earth 'Protect-it' was assessed in a farm scale experiment. The surface of a mite-infested 20 t bin was divided into quadrants. Two were treated with 1g/kg of 'Protect-it' and two were left untreated. The mite population at the surface of the treated quadrants fell to near zero within a fortnight, although the effect at a depth of 0.25m was much less marked.

This project has demonstrated that there are potential alternative compounds to OPs that have proved effective against storage mite and insect pests. Most of the compounds were very effective as protectants, inhibiting the development of pest populations. However, some did have limitations in treating existing infestations, either because they worked rather slowly or because they were less effective against certain stages or species. They may prove suitable as admixture treatments to protect unventilated grain during prolonged storage or as a surface treatment in conjunction with cooling and drying, to combat the peculiar problems of the British maritime climate. However, if used as infestation treatments, for instance during loading at ports, careful selection of the compound may be required depending on the infestation present.

The availability of any new compounds as grain protectants will be largely determined by the registration process, the small U.K. market and the cost of registration. Of the compounds tested, the nearest to the market are the diatomaceous earths which are registered for storage use in other countries, have the advantage of a physical mode of action and have been tested under U.K. conditions against insects and mites.

The future of any potential replacements to OPs lies in their ability to be incorporated into an integrated pest management programme. A targeted approach may be required where knowledge of the environment and pest biology are important factors in deciding the appropriate control measure, with a move away from sole reliance on one method.

BACKGROUND INFORMATION
Mites are very common pests of stored grain and oilseeds in the U.K. A survey of commercial grain stores during 1988/89 and oilseed stores in 1995, detected the presence of mites in 81.3 % and 89 % of the stores respectively (Lynch et al., 1991; Prickett, 1997). The most common species in the grain stores were Acarus siro, Lepidoglyphus destructor, Tyrophagus longior and Tyrophagus putrescentiae, identified in 59%, 51.2%, 15.9% and 12% of stores respectively (Lynch et al., 1991). In the oilseed stores the predominant species were Acarus siro (67%), Lepidoglyphus destructor (37%), Tyrophagus putrescentiae (31%) and Tyrophagus longior (19%) (Prickett, 1997).

Some mites feed on the germ of cereals (Solomon, 1946) and hollow out rapeseed leaving only the seed coat (Anon, 1982), thus destroying germination capacity and decreasing the value for seed and malting. Heavy infestations can have a strong smell which taints the grain, making it unpalatable to livestock and unsuitable for milling (Wilkin and Stables, 1985). Research has found reduced growth rates in pigs fed a diet heavily infested with mites (Wilkin and Thind, 1984). Mites in finished cereal products are also a cause of concern. A recent investigation found 22% of cereal based products contained at least one mite (Anon, 1996). Infestations may arise as a result of mites entering the product during any stage in its manufacture, transport and storage (Anon, 1996). Mites are also highly allergenic and can pose a serious health risk to workers involved in grain and flour handling (Stengard Hansen et al., 1996). They have also been implicated in the transmission of micro-organisms, especially fungi, with recent suggestions of a role as vectors of prions (Sigrianskii, 1940; Griffiths et al, 1959; Wisniewski et al., 1996).

There is a requirement for traded grain to be pest-free; EC regulation 689/92 states in Article 2, that to be accepted for intervention, 'cereals must be free from live pests (including mites) at every stage of their development' (Intervention Board, 1996). In the U.K. stored grain protection has relied heavily on bulk admixture with insecticides. A survey of commercial grain stores in 1988/89 found that 67.5% of the sites had used contact pesticides on all or part of the grain, with two thirds treating for prophylactic reasons (Prickett, 1991). The only contact pesticides approved for use on stored grain are the organophosphorus (OP) compounds pirimiphos-methyl (Actellic), etrimfos (Satisfar ) and chlorpyrifos-methyl (Reldan) (Whitehead, 2000). The survey of commercial stores found that pirimiphos-methyl, chlorpyrifos-methyl and etrimfos had been used in 73%, 21% and 12% of sites that treated grain, respectively (Prickett, 1991). With oilseeds, however, pirimiphos-methyl lost its approval for use on the commodity earlier this year, leaving the fumigant phosphine as the only pesticide available for oilseed treatment (Abel, 2000).

However, none of the OPs are particularly effective against field strains of mites. Results from recent surveys have found widespread resistance in populations of Acarus siro to one or more of these compounds. Resistance to twice the recommended rate of pirimiphos-methyl was detected in 15% of Acarus siro strains from farm stores (1987), 71% of strains from commercial stores (1988/89), 91% from animal feed mills (1992) and 93% from oilseed stores (1995) (Starzewski, 1991; Prickett, 1994; Prickett, 1997). In the latter survey resistance to chlorpyrifos-methyl was also detected in 63% of stores but only in mites from stores where pirimiphos-methyl resistance was found (Prickett and Buckland, 1997). Resistance to etrimfos was also detected in two pirimiphos-methyl resistant strains (Prickett and Buckland, 1997). Unpublished data from the Central Science Laboratory by Binns and Buckland, found one Acarus siro population from a commercial store to be resistant to pirimiphos-methyl, etrimfos and chlorpyrifos-methyl.

Thind et al. (1996) also detected cross-resistance to chlorpyrifos-methyl and etrimfos in a pirimiphos-methyl resistant field strain of Lepidoglyphus destructor. This suggests that resistance to OPs in this case, has conferred cross-resistance to all three compounds, and it is possible that a single mechanism is responsible (Thind et al., 1996). Therefore, the use of any one compound may lead to selection for resistance to the others. Resistance to pirimiphos-methyl has been linked to an increase in esterase activity but other mechanisms may also be involved (Szlendak et al., 2000).

As well as concerns regarding the development of resistant pests, the costs and consumer resistance to toxic chemicals in food, have led to increasing pressures for a reduction in pesticide use. There are also strong pressures for OPs to be replaced, which can be based on fears that they may cause Chronic Fatigue Syndrome (CFS) following use as sheep dips, be involved in Gulf War Syndrome, have a causal link to spongiform encephalitis by causing prion mutation, or be a trigger for autoimmune diseases amid the continuing concerns over their undoubted presence as residues in foodstuffs (Vial et al., 1996; Wester et al., 1996; Stephens et al. 1996; Fairhall, 1996; Davies, 1997; Warden, 1996).

Cooling and drying can be used effectively to protect grain from pest infestation. By reducing the temperature of grain to below 5oC mite breeding is prevented; and by drying grain to below 60% rh development can be inhibited (Cunnington, 1976). However, during the winter the surface layers may reabsorb moisture from the atmosphere (Burrell and Havers, 1976) locally increasing product moisture content and enhancing the development of surface mite infestations (Armitage, 1984). Surface grain cannot be kept cool or dry enough to limit mite numbers, so a surface pesticide treatment may be required.

There are a number of alternative compounds used effectively against acarine pests in field agriculture, veterinary and public health control programs, which may also prove effective against storage mites. These include insect growth regulators, inert dusts, botanicals, novel compounds and biological control agents. This project aims to identify potential alternatives to OPs and to investigate their efficacy against storage pests with a view to their use within an integrated pest management program.

Conclusions

Most of the compounds assessed were very effective as protectants, inhibiting the development of pest populations. However, some had limitations in treating existing infestations, either because they worked rather slowly or because they were less effective against certain stages or species. The most successful were the chitin synthesis inhibitor, flufenoxuron, the plant extract, azadirachtin and the diatomaceous earth, 'Protect-it'. This last-named compound was successfully applied as a top dressing against an existing heavy mite infestation.

Implications
These experiments have enabled the benefits and limitations of the available alternatives to be clearly identified. They are effective in inhibiting the development of infestation but have limitations if a broad spectrum of pests require to be killed quickly. Their use may therefore lie in an integrated approach when applied as fabric treatments or as a top dressing, in conjunction with cooling and drying. However, if used as infestation treatments, for instance during loading at ports, careful selection of the compound may be required depending on the pest species present. The availability of any new compounds as grain protectants will be largely determined by the registration process, the small U.K. market and the cost of registration. Of the compounds tested, the nearest to the market are the diatomaceous earths which have the advantage of a physical mode of action and which have been extensively tested under U.K. conditions against insects and mites.

Abstract

Aims
This project aimed to find alternative compounds to organophosphorus (OP) pesticides for the control of storage mite pests from readily-available commercial formulations in a number categories, based on their activity; growth regulators, pyrethroids, diatomaceous earths, compounds of biological and novel control agents and botanicals. The initial aim was to screen 21 compounds for activity against mites, and then narrow the focus by ensuring that the most promising six were effective against stored product insects as well as mites under U.K. conditions. The final aim was to test the most successful candidates against mixed infestations on a larger scale culminating with a farm-scale trial and to ensure they were equally efficacious on rapeseed.