Pheromone use in the food industry

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ing the protozoan pathogen Mattesia spp, subsequently transmitting the disease to over 90% of a test population. Using phe- romone-baited spore-transfer sites ...
Pheromone use in the food industry Dr M. N. Hassan and Dr Shakir Al-zaidi*

A pheromone is a chemical signal secreted by an organism into the environment that causes a specific reaction when detected by another individual of the same species. A sex pheromone is used to help one sex orient toward and find the other sex for mating. Insects can detect sex pheromone over a long distance on wind currents and responded by flying upwind to the source of the pheromone ‘plume’. In most cases, the female insect secretes a sex pheromone and the male flies in response to locate the female. These are the most widespread and widely documented types of pheromone. Aggregation pheromones are emitted by one sex and attract both sexes to a food source or for mating, eliciting movement towards the source over a long distance (low pheromone concentration) and arrestment on arriving close to the source (high pheromone concentration). The first pheromone to be identified was the sex pheromone of the silkworm moth, Bombyx mori, in 1959. Since then, sex pheromones have been identified in several hundred species of Lepidoptera and other orders, while aggregation pheromones have been identified for hundreds of species of Coleoptera, Dictyoptera, Hemiptera, Homoptera and Orthoptera. Pheromones are volatile compounds, highly biologically active and effective at low concentrations, and they are non-toxic to plants and animals. It is now well recognized that synthetic pheromones could be used as effective behaviour modifying tools for insect pest management. Insects have been an integral problem in stored food grains throughout history with earliest evidence from archaeological deposits. Once harvested, food grains and dry food products have to pass though a number of processes before reaching the consumer as a processed food. Stored grain is susceptible to insect infestation owing to high grain temperatures and moisture along with

*Russell IPM Ltd, Unıt 68,Thırd Avenue, Deesıde Industrıal Park,Flıntshıre CH5 2LA, UK; Email: nayem@russellıpm.net

broken kernels which allow them to gain entry. Some insects can be transferred to stored grain from the field or via infested grain bins. Protection of stored food from insects is necessary because of the large quantities they can destroy, particularly during long-term storage. Historically, stored product insect control has mainly relied on the use of chemical admixtures and fumigation and this continues today. However, although chemical insecticides are effective and can control the insects, they pose risks to human health and the environment and also kill natural enemies of the pests. Alternative approaches are needed for controlling stored product insects. Pheromones could be used in a number of ways (in mass trapping, mating disruption) or in combination with entomopathogens to provide a sustainable, eco-friendly and effective biological control measure for stored product insects. Sex pheromones for monitoring

The most successful and widespread use of pheromones has been in monitoring traps. Monitoring traps consist of cardboard or plastic devices that contain a pheromone emitter and a sticky surface. A male moth, fooled into thinking that the emitter is a female releasing a pheromone, flies into the trap and is caught on the sticky surface. Synthetic pheromones are now used in a variety of traps as detection and monitoring tools in pest management programmes. Other traps that use non-pheromone food baits to attract insects are also used. The first stored product insect pheromone was chemically identified in 1966 from the black carpet beetle, Attagenus unicolor1, and since then 40 stored product insect pheromones have been identified. In terms of stored product pests, sex pheromones are produced by pyralid and gelichiid moths and by several species of beetles in the families Anobiidae, Bruchidae and Dermestidae. The adults of these species are typically short-lived compared with other stored products insects. Male beetles in the families

Bostrichidae, Cucujidae, Curculionidae, Silvanidae and Tenebrionidae produce aggregation pheromones, and adults of these species are typically longlived relative to the sex pheromone producing species. Phillips2 reported that feeding is required by males to produce aggregation pheromone, and an optimum response from females and males is achieved when the aggregation pheromone is released together with food odours. Landolt3 found that female moths that are secreting sex pheromones also utilize male-produced attractants and similarly many beetles with male-produced aggregation pheromones clearly utilize female-produced sex attractants in certain contexts. Combination of semiochemicals

A combination of aggregation pheromone and food attractant can provide an effective monitoring tool for stored product insects. Some traps are designed so the pheromones for more than one species can be used at the same time. The presence of several pheromones in one trap has three possible outcomes. First, an insect may be attracted by its own pheromone regardless of the other pheromones. Second, the attraction may be greater due to the combination of its pheromone with that of another species. Finally, the attraction may be reduced due to repellent characteristics of a pheromone from another species4. The interaction of pheromones and food attractant in the same trap and the resulting influence on the trap catch are important when monitoring for several insect species. Dowdy and Mullen4 reported the effect of the paired interaction of synthetic pheromones used in the same trap on the effectiveness of trapping Rhyzopertha dominica, Tribolium castaneum and Trogoderma variabile. The R. dominica pheromone can be used in a trap together with pheromones for Tribolium castaneum and Trogoderma variabile. The pheromone of T. variabile does not appear to impact adversely on the trap catch of Tribolium castaneum. Laboratory tests indicate that pheromones for the rusty grain beetle

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(Cryptolestes ferrugineus) and red flour beetle (T. castaneum) can be used in the same trap without reducing the attractancy of the trap for either species, and there is even a slight cross attraction of the red flour beetle to the rusty grain beetle pheromone5. Russell IPM developed a very effective multi-species commercial pheromone trap, Xlure-MST, by integrating two synthetic pheromone lures and three food attractants for Tribolium spp. (red and confused flour beetles, T. castaneum and T. confusum), Lasioderma serricorne (cigarette beetle), Trogoderma granarium (khapra beetle) and T. variabile (warehouse beetle). Xlure-MST is a powerful multi-species trap capable of detecting crawling beetles and weevils in its vicinity. Using a single trap to monitor ten insect species will result in reduced costs and reduced labour in maintaining pest surveillance programmes in the food industry. In developing a trapping strategy for pest control in the food industry, the first step is to consider the advantages and demands of a multi-species trap concept. 1. It will offer a broad spectrum screening tool which puts all potential insect pests on the radar screen. 2. It will be more cost effective than using many traps for different insects. 3. It will reduce the time required to monitor and service traps. 4. A truly multi-species trap should be able to cover the entire spectrum of insects entering the food chain at every stage if it is to provide a single tool which can be used by all involved in the food chain to help compare data and pinpoint areas of weakness.

5. Although the issue of pests in the food chain is looked at differently by different stakeholders, it will be necessary for all of them to accept a single and jointly accepted yardstick in order to compare findings. In a laboratory bioassay, the efficacy of the Xlure-MST trap was evaluated against Tribolium castaneum. The results indicated that Xlure-MST is attractive to T. castaneum, with a mean catch efficacy of more than 80% after 24 hours (see Figure 1). It also showed that once the beetles are caught in the trap they are unable to escape from it again. The slope of the trap does not present an obstacle to the ease of entry by the beetles into it. Xlure-RTU is another multi-species trap developed by Russell IPM for flying insects in the food industry, e.g. Indian meal moth (Plodia interpunctella), mill moth (Ephestia kuehniella), tropical warehouse moth (E. cautella),

Plate 1. Cross section of Xlure-MST trap showing pheromone and food attractant in one trap.

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Pheromones

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jFood (attractant)

warehouse moth (E. elutella), cigarette beetle (Lasioderma serricorne) and warehouse beetle (Trogoderma sp.) Mass trapping

Mass trapping is a technique that involves placing a high number of traps in various strategic positions to remove a sufficiently high proportion of individuals from a pest population to achieve the required level of protection. Laboratory-based studies on mass trapping suggested this technique would not be effective for stored product insects because of the poor catches possibly associated either with early trap designs or the presence of contaminating isomers in the lure6. However, FleuratLessard et al.7 reported that mass trapping of the moth Plodia interpunctella with pheromones in a French seed store over several years resulted in a considerable reduction in infestation and the need for insecticide treatments. A major limitation with female-produced sex pheromones, which are most commonly used in storage systems, is that only males are trapped. In species where males mate many times, up to 90% of the male population can be trapped without affecting the number of mated females and thus the subsequent larval generation. To be effective, mass trapping must ensure that a high proportion of female pests are either trapped or left unmated8. Mass trapping both sexes of a population using aggregation pheromones should be more effective9. Aggregation

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pheromones produced by males are known from several beetle species that infest stored products. Suzuki and Sugawara10 reported laboratory studies in which both sexes of T. castaneum respond to the male-produced aggregation pheromone. Similarly, Chambers et al.11 reported that male Sitophilus granarius produce an aggregation pheromone. The application of pheromone traps to control insect pests by mass trapping has been particularly successful against Coleoptera using traps baited with aggregation pheromones. This involves deploying pheromone traps at a much higher density than for monitoring purposes. Mass trapping of Lasioderma serricorne in Greek tobacco stores using the sex pheromone on multi-surface sticky traps removed over 500,000 male beetles during a 15 month period, nearly four times as many beetles as traps without pheromone12. Aggregation pheromones have more potential than sex pheromones for mass trapping based control of insect pests in stored products. However, further experimental evaluation is required. Mating disruption

The mating disruption technique (also known as sexual confusion) is the most widespread application of pheromones in insect pest management: laying of fertilized eggs by the female is minimized or prevented by interfering with successful mating between male and female insects. For practical pest control, the technique of mating disruption generally requires the use of much larger quantities of semiochemicals than does mass trapping8. The mechanisms involved are not completely understood13,14, but the three most likely modes of action are: 1. Adaptation of the antennal receptors and habituation of the central nervous system, caused by the continuous exposure of insects to a relatively high concentration of pheromone, which prevents the insect responding to a potential mate. 2. Camouflaging of the natural pheromone plume from a calling mate resulting from the use of a high background level of pheromone which renders trail-following impossible. 3. False-trail following when a relatively large number of point sources

of pheromone are spread around an area to present the pest male with many false trails. The efficacy of this technology is related to the motility of mated females into the area to be managed, the initial population levels of the pest, the release characteristics of the formulation and implementation of a sophisticated management programme. In the case of Plodia interpunctella and Ephestia cautella, mating was substantially reduced in the presence of synthetic sex pheromones in simulated storage15. Mating frequencies in E. cautella were reduced from 56–70% in untreated controls down to 4–38% in the presence of the synthetic pheromone, with greatest reductions occurring at the lowest moth population densities (0.1 moths/m2 of surface). For both species of moth, use of the synthetic pheromone effectively limited population growth when applied to low populations but not when high densities of moths were present. Significant mating disruption and population reduction of E. cautella at low moth densities in the laboratory and in cocoa stores by microencapsulated formulations was reported by Hodges et al.16. Integration of entomopathogens and semiochemicals

The application of micro-organisms is a promising alternative to the use of conventional pesticides for protection of stored products. A variety of ento-

mopathogens are used to control invertebrate pests in stored products. The advantages of using entomopathogens in this context are safety for humans and other non-target organisms (natural enemies), which also usually facilitates increased activity of other natural enemies. Early attempts to control species of stored products pests using semiochemicals to attract them to a source of protozoa included Burkholder and Boush17 who attracted the dermestid beetle Trogoderma glabrum to a pheromone source containing the protozoan pathogen Mattesia spp, subsequently transmitting the disease to over 90% of a test population. Using pheromone-baited spore-transfer sites under simulated warehouse conditions male populations of T. glabrum were reduced to below pre-treatment levels by the second generation after treatment18. However, these pathogens suffer the possible disadvantage of being too species-specific to make them effective in a management strategy for storage environments where a number of different pest species are often present8. More recently, vegetable fat pellets containing aggregation pheromone and the entomopathogenic fungus, Beauveria bassiana, have been used in laboratory tests to attract and kill Prostephanus truncatus19. The method showed promise for the control of this beetle in maize stores and has the additional advantage that using the fat pellet formulation avoids any possible allergen hazard associated with the presence of airborne fungal conidia.

Plate 2. Xlure-MST trap in use in the food industry

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Entomopathogenic nematodes have been used to control members of some of the major pest families encountered in storage commodities including pyralid moths and curculionid beetles. Ramos-Rodriguez et al.20 investigated nematodes, Steinernema spp., as biological control agents against larvae, pupae and adults of six stored product pest species (Plodia interpunctella, Ephestia kuehniella, Oryzaephilus surinamensis, Tenebrio molitor, Tribolium castaneum and Trogoderma variabile) and adults of two additional species (Sitophilus oryzae and Rhyzopertha dominica). They obtained promising results, including 80% or higher mortality against larvae of P. interpunctella with one Steinernema species. There are challenges to using entomopathogenic nematodes, in terms of providing the film of moisture essential for their survival. However, recent research shows that the nematodes can survive in cryptic habitats and warm conditions. Some species can tolerate soil up to 35ºC and have been used to control insects in cryptic environments outside the soil. For example, S. carpocapsae has been used for controlling cockroaches. Combined deployment of pheromones and entomopathogenic nematodes in a single trap is a potential biological control approach for exposing stored product insect pests to entomopathogens. One possible approach would involve including pheromone traps as part of a bait station. Adult insects would follow the pheromone plume into the trap, where they would come in contact with an entomopathogenic source. The entomopathogens would adhere to the visiting insect and subsequently infect and kill it. Either the entomopathogenic fungus Beauveria bassiana or the entomopathogenic nematodes could be used in association with a pheromone in this way. In addition to becoming infected itself, the insect could be a carrier of the pathogens, and disseminate them to the opposite sex on mating. Further work is needed to optimize integration of semiochemicals and entomopathogens for controlling stored product insects. References 1 Silverstein R.M., Rodin J.O., Burkholder W.E. and Gorman J.E. (1967) Sex attractant of the black carpet beetle. Science 157, 85–87.

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2 Phillips, T.W. (1997) Semiochemicals of stored product insects: research and application. Journal of Stored Products Research 33, 17–30. 3 Landolt, P.J. (1997) Sex attractant and aggregation pheromones of male phytophagous insects. American Entomologist 43, 12–22. 4 Dowdy, A.K. and Mullen, M.A. (1997) Multiple stored-product insect pheromone use in pitfall traps. Journal of Stored Products Research 34, 75–80. 5 Lindgren, B.S., Borden, J.H., Pierce, A.M., Pierce, H.D., Jr., Oehlschlager, A.C. and Wong, J.W. (1985) A potential method for simultaneous, semiochetnical-based monitoring of Cryptolestes ferrugineus and Tribolium custaneum (Coleoptera: Cucujidae and Tenebrionidae). Journal of Stored Products Research 21, 83–87. 6 Bommer, H. and Reichmuth, C. (1980) Pheromone der vorratssch.adlichen Motten in der biologischen Sch.adlingsbek- ampfung. Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft (198), 114 pp. 7 Fleurat-Lessard, F., Siegfried, M. and Le Torc’h, J. (1986) Utilisation d’un attractif de synthèse pour la surveillance et le piégeage des pyrales Phycitinae dans les locaux de stockage et de conditionnement de denrées alimentaires végétales. Agronomie 6, 567–573. 8 Cox, P.D. (2004) Review potential for using semiochemicals to protect stored products from insect infestation. Journal of Stored Products Research 40, 1–25. 9 Trematerra, P. (1997) Integrated pest management of stored-product insects: practical utilization of pheromones. Anzeiger f .ur Sch.adlingskunde Pflanzenschutz Umweltschutz 70, 41–44. 10 Suzuki, T. and Sugawara, R. (1979) Isolation of an aggregation pheromone from the flour beetles Tribolium castaneum and T. confusum. Applied Entomology and Zoology 14, 228–230. 11 Chambers, J., Van Wyk, C.B., White, P.R., Gerrard, C.M. and Mori, K. (1996) Grain weevil, Sitophilus granarius: antennal and behavioural responses to maleproduced volatiles. Journal of Chemical Ecology 22, 1639–1654. 12 Buchelos, C.T. and Levinson, A.R. (1993) Efficacy of multisurface traps and Lasiotraps with and without pheromone addition, for monitoring and mass-trapping of Lasioderma serricorne in insec-

Plate 3. A multi-species trap for flying stored product insects, Xlure-RTU

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ticide-free tobacco stores. Journal of Applied Entomology 116, 440–448. Campion, D.G., Critchley, B.R. and McVeigh, L.J. (1989) Mating disruption. In: Insect pheromone in plant protection, Jutsum, A.R. and Gordon, R.F.S. (eds), pp. 89–116. John Wiley and Sons, Chichester, UK. Cardé, R.T. and Minks, A.K. (1995) Control of moth pests by mating disruption: successes and constraints. Annual Review of Entomology 40, 559–585. Sower, L.L. and Whitmer, G.P. (1977) Population growth and mating success of Indian meal moths and almond moths in the presence of synthetic sex pheromone. Environmental Entomology 6, 17–20. Hodges, R.J., Cork, A. and Hall, D.R. (1984) Aggregation pheromones for monitoring the greater grain borer Prostephanus truncatus. In: Proceedings of the British Crop Protection Conference, Brighton, UK. pp 255–259 Burkholder, W.E. and Boush, G.M. (1974) Pheromones in stored product insect trapping and pathogen dissemination. Bulletin of the OEPP 4, 455–461. Shapas, T.J., Burkholder, W.E. and Boush, G.M. (1977) Population suppression of Trogoderma glabrum by using pheromone luring for protozoan pathogen dissemination. Journal of Economic Entomology 70, 469–474. Smith, S.M., Moore, D., Karanja, L.W. and Chandi, E.A. (1999) Formulation of vegetable fat pellets with pheromone and Beauvaria bassiana to control the larger grain borer, Prostephanus truncatus. Pesticide Science 55, 711–718. Ramos-Rodriguez, O., Campbell, J.F and Ramaswamy, S.B. (2006) Pathogenicity of three species of entomopathogenic nematodes to some major stored-product insect pests. Journal of Stored Products Research 42, 241–252

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