Management of the diamondback moth: déjà vu all over again?

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1 Management of the diamondback moth: déjà vu all over again? A.M. Shelton Department of Entomology, Cornell University/New York State Agricultural Experiment Station, Geneva, New York, 14456, USA Abstract The diamondback moth, Plutella xylostella (L.), is considered the most universally distributed of all Lepidoptera and the main insect pest of crucifers worldwide. Although P. xylostella is confined to feeding on plants within the Cruciferae, this diverse family contains a wide host of weed species and cultivated plants that occur throughout the world. Over the last several decades the importance of crucifers in the human diet has increased, resulting in increased crucifer production and changing management practices. Where once crucifers were part of smaller diversified cropping systems, they are often now grown as monocultures under intensive cultivation practices, including year-round production. In areas of China, south-east Asia and other areas where crucifers are important to the human diet, there may be more than 20 generations of P. xylostella annually. As production practices have changed and the demand for damage-free produce has intensified, farmers have relied on intensive use of insecticides which, in turn, has contributed to insecticide resistance, reduced effectiveness of natural enemies, frequent control failures, and some environmental and human health concerns. Because of the health benefits and cultural significance of crucifers, especially in Asian populations, production will continue to increase. What have we learned from the past that will allow us to provide better management of P. xylostella in the future? A central element will be to develop preventative tactics and rescue treatments which conserve natural enemies, promote resistance management strategies, and utilize cultural control practices that rely on understanding the agroecology of P. xylostella. Most importantly, successful management of P. xylostella will rely on farmers and scientists taking a more regional perspective that includes information on P. xylostella movement and the effects of management tactics on their behaviour and population genetics on a community level. Keywords Plutella xylostella The importance of the diamondback moth Throughout the world the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), is considered the main insect pest of crucifers, particularly cabbages, broccoli and cauliflowers (Talekar & Shelton 1993). Plutella xylostella is considered the most widely distributed lepidopteran pest, and occurs in diverse small scale and large scale agricultural production areas, as well as on weeds. A decade ago, Javier (1992) estimated the cost for controlling it at US$1 billion annually, but it is unclear how this cost was calculated. The economic impact of P. xylostella can be evaluated by several methods. If one determines the potential value of the crop, the potential loss incurred if insects made the plant totally unmarketable, the cost of control to prevent it from being unmarketable, then the actual value of the crop minus the cost of control can be calculated as the loss caused by the insect. However, a plant will often not be made fully unmarketable, but may be reduced in yield or quality and require additional trimming to remove the damage. Furthermore, additional complications arise due to the large number of insecticides used against P. xylostella, their variable costs, the variable number of applications and their effectiveness. Further complications arise since some applications on crucifers may be targeted against other insect pests such as aphids or other Lepidoptera. Thus, there does not appear to be any reliable data on the total worldwide value of crucifers nor the losses incurred by P. xylostella. However, the following examples give some indication of the importance of P. xylostella in selected regions of the world (Shelton 2001). China has the largest population in the world and cruciferous vegetables make up an important part of the Chinese diet. The area of cabbage and cauliflower grown in 1999 in China was 1.2 million ha. (FAO 2001) and P. xylostella is widespread in most provinces. There are five or six generations in Jilin Province in Northeastern China and up to 20 generations in Guangdong Province in Southern China. Plutella xylostella has been the most important insect pest of cruciferous vegetables especially in Southern China and the Changjiang River Valley in the last 20 years. When no sprays were applied to control P. xylostella, the losses Proceedings of the 4th International Workshop, Nov. 2001, Melbourne, Australia 3

2 of summer cabbage in Shanghai were 99% in 1992 and 80% in 1994, compared with the plots treated with insecticides (Zhao et al. 1996). The estimated control costs are ca. US$100/ha for each crop for the peak periods (in April/May and September/October). In the United States and Canada, the importance of P. xylostella is variable. Nearly 6 million ha of canola are grown in Canada and, in 1995, ca million ha were sprayed to control an outbreak of P. xylostella at an estimated cost of CN $50 million (Dosdall et al. 2004). In Texas it has been suggested that 100% of cabbage and at least 20% of broccoli would be unmarketable if it were not treated (T.X. Liu, personal communication). This translates to losses of $40M - $70M for cabbage and ca. $400K for broccoli. A similar situation also occurs in Florida where P. xylostella is the main pest of crucifers. In the more northerly latitudes of the US, the situation is different because of less pressure by P. xylostella. Cathy Eastman in Illinois (personal communication) notes that cruciferous vegetable crops are grown on ca. 30,000 acres in the Midwest and > 80% of the acreage needs to be treated at least once for the P. xylostella and P. rapae complex. Depending on the season, most growers may treat 2-3 times for this complex. This is the same situation noted by A. M. Shelton in New York, although during hot, dry years P. xylostella will be a much more difficult problem and, if no treatments are applied, much of the ca. $80 million cabbage crop would be unmarketable for fresh market cabbage. California is a main US producer of fresh market broccoli where it was grown on nearly 50,000 ha with a farm gate value of ca. $500 million. A severe infestation by P. xylostella in 1997 resulted in crop losses estimated to be > $6 million (Shelton et al. 2000). Mexico is a major producer of broccoli and related crucifers used for processing and export to the United States. Most production is located in the El Bajio region where more than 30,000 ha of broccoli are produced with a total farm gate value of >US $63 million. Plutella xylostella greatly reduces the yield and quality of the crop and accounts for the majority of insecticide use in crucifer production (Diaz-Gomez et al. 2000). If no sprays were applied for control of P. xylostella, it is reasonable to conclude that all plants would be unmarketable. In Australia, Greg Baker (personal communication) notes that P. xylostella attacks the 136,000 hectares of major Brassica vegetable crops and is considered the chief insect pest. Crop loss due to P. xylostella damage in an average year is estimated to be ca. $A 8 million and control costs $A 12 million. Another important crop attacked by P. xylostella is canola and in Australia there is ca. 1 million ha. The crop loss in canola due to P. xylostella is estimated to be ca. $A 3 million and control cost $A 6 million. Throughout Europe, P. xylostella attacks Brassica vegetables and field crops such as canola on a regular basis. These crops are grown throughout Germany with high concentrations of cabbage and canola in the northern parts of Germany. Cruciferous vegetables amount to one third of the total field vegetable growing area in Germany. There are no comprehensive data on yield losses due to P. xylostella attack but, in most years, the attack level by P. xylostella will be below an injury level and the pest will be controlled by spraying against the other two main lepidopteran pests, Pieris rapae and Mamestra brassicae (Martin Hammes, personal communication). In some years, particularly during hot, dry weather conditions, heavy attack and corresponding high yield losses can be observed. This situation is very similar to the Netherlands where 8,500 ha of cabbages and cauliflower are grown. Other large producers of cabbages and cauliflower are India (530,000 ha), Russian federation (162,700 ha), South America (7,000 ha) and the combined area of Indonesia, Thailand and Vietnam which have a total of 78,655 ha (FAO 2001). Other cruciferous crops are also attacked by P. xylostella, but the value of these crops is unknown. Losses caused by P. xylostella in all these areas, especially in southeast Asia, can be very severe since P. xylostella has developed resistance to many insecticides (Talekar & Shelton 1993). Because of the importance of P. xylostella, the pest was the subject of three international conferences prior to this meeting. The first two were held in Taiwan in 1985 and 1990, respectively, while the third was held in 1996 in Malaysia. It is important to note the changing emphasis of the talks over the three conferences with a marked trend for more presentations on biological control, insecticide resistance and IPM. The third and this present conference continue that appropriate trend. Crucifers, humans and the history of P. xylostella problems The history of P. xylostella is associated with the history of its diverse host crops. Plutella xylostella is restricted to the plant family Cruciferae, although a recent report has indicated that a population in Kenya 4 Proceedings of the 4th International Workshop, Nov. 2001, Melbourne, Australia

3 can survive on peas (Bernhard Löhr, personal communication). However, this example seems like an anomaly due to growing peas nearby crucifers. There are 220 genera of crucifers, which include many wild and cultivated plants, and they occur on all continents. Crucifers are characterised by a wide range of secondary plant compounds (glucosinolates) toxic to many insects, although the specialist P. xylostella has come to rely on some of them for host location and feeding. The glucosides sinigrin, sinalbin and glucocheirolin act as specific feeding stimulants for P. xylostella and 40 plant species containing one or more of these chemicals serve as hosts (Talekar & Shelton 1993). Non-host plants may contain these stimulants, but also contain feeding inhibitors or toxins (Gupta & Thorsteinson 1960). Allyl isothiocyanate also stimulates egg production in P. xylostella adults (Hillyer & Thorsteinson 1969). Cruciferous vegetables, primarily brassicas, are important components of the human diet and are grown on small subsistence farms as well as large scale farms. In 2000, over 3.5 million ha of cabbages were harvested worldwide and these cabbages included Chinese cabbage, mustard cabbage, pak choi (Brassica chinensis), white and red cabbages, Savoy cabbages, Brussels sprouts, collards, kale and kohlrabi (FAO 2001). An additional 834,000 ha of broccoli were produced. These cruciferous vegetables are important component of the Asian diet and nearly 50% of them are produced in Asia, where loose-leafed cabbages are preferred. Modern hard-headed cabbages descended from wild cabbages that originated in the Mediterranean and Asia Minor. Wild cabbages were called gifts from the Gods and the Celts and Romans spread them throughout Europe. These cabbages were introduced into North America by early explorers in More recently, canola or rapeseed has become a major cruciferous crop with greater than 12 million metric tonnes produced in 2000 (FAO 2001). Products from canola/rapeseed include oils for human consumption, industrial oils and animal feeds. With the growth in area of canola/rapeseed, reports of problems of P. xylostella management have been reported in Canada, Australia and Europe. While P. xylostella and crucifers have existed for centuries, it is clear that in many areas of the world there is greater concern about P. xylostella causing economic damage to crops. There are several potential reasons for this. In the US it has been estimated that 39% of our pests were brought over with the new crops, while in South Africa it has been estimated that 68% of the 188 arthropod species on 14 introduced crops switched hosts once another suitable host was introduced (Van Driesche & Bellows 1996). Clearly, the introduction of a new crop into an area can lead to insect pest problems. However, it is unlikely, for a number of social and economic reasons, that growing plants in a potentially suitable region will be restricted in the future so this will not be a realistic method for P. xylostella management. However, other human agricultural practices have caused large consequences for P. xylostella, and these are the ones that we may be able to help manage in the future. We have abundant evidence that P. xylostella problems have been exacerbated by the use of year-round crucifer cultivation which eliminates a break in the insect cycle. This practice, combined with an overuse of insecticides, often leads to control failures. There are more than 500 cases of arthropods becoming resistance to a particular pesticide (Georghiou & Lagunes-Tejeda 1991) and P. xylostella is one of the leaders in this area. Plutella xylostella is the first agricultural insect to have developed resistance to DDT (Ankersmit 1953, Johnson 1953) and, since that time, some populations of P. xylostella in certain areas have developed resistance to all known classes of insecticides. This includes resistance to Cry1A and Cry1C toxins of the bacterium, Bacillus thuringiensis, in many places (Shelton & Roush 2000) and, to a far lesser extent, to spinosad in specific areas of Hawaii (Zhao et al. 2002). Prior to the introduction of pyrethroids in the early 1980s, the main classes of insecticides used for P. xylostella control were organophosphate and carbamate insecticides. Although pyrethroids have a higher level of safety for humans, there are other problems. Pyrethroids are fairly broad spectrum and their use often disrupts natural enemies because they are usually more susceptible than the pest species (Croft & Brown 1975, Croft 1990). In one of our recent works, we examined the potential to integrate biological and insecticidal control of P. xylostella with Diadegma insulare (Cresson) (Hymenoptera: Ichneumonidae), one of the most important parasitoids of P. xylostella in North America (Harcourt 1986, Lasota & Kok 1986, Hu et al. 1998, Shelton et al. 2002). Our results (Xu et al. 2001) indicate that D. insulare increases its tolerance to permethrin much more slowly than P. xylostella and appears limited in the extent of resistance it can develop. For example, we can often find populations of P. xylostella with several hundred-fold resistance to permethrin, but we were only able to detect a 5-fold level of tolerance in D. insulare. Thus, rather than building up tolerance in a parasitoid or predator of P. xylostella, it may be more appropriate to use an insecticide which will have less impact on the parasitoid in the first place. Compared with the organophosphates, carbamates and pyrethroids, materials such as Bt, spinosad, indoxacarb and emamectin Proceedings of the 4th International Workshop, Nov. 2001, Melbourne, Australia 5

4 benzoate are generally considered less harmful to natural enemies. Additional studies are being performed in various laboratories to determine their impact on natural enemies of P. xylostella under field conditions and this type of information is sorely needed. The future for managing P. xylostella As has been written, Past experiences with diamondback moth management have reinforced the belief that single component strategies will fail and we need to rely on other cultural and biological controls to a greater degree (Talekar & Shelton 1993). What is needed is an integrated approach using host plant resistance, biological controls, cultural controls, behavioural management and judicious use of insecticides. None alone will work sufficiently, but together they can complement each other and lead to a more sustainable system. However, underlying all of these strategies must be a more complete understanding of the movement patterns of P. xylostella and the causes that influence movement. To develop sound management strategies for P. xylostella will require an understanding of the ecology of the landscape in which P. xylostella and its natural enemies interact with the rest of this agroecosystem. We really know very little about movement of P. xylostella, although there are scattered reports that it can move long distances (Chu 1986). For P. xylostella adults, the spatial and temporal relationship of cruciferous weeds and crops, and wind patterns will influence movement and the probability of infestation. The scale of the movement can be local (within an individual field or between adjacent fields), or regional or intercontinental. Perhaps little can be done to prevent regional movement of P. xylostella other than to ensure they are not being transported on transplants (Shelton et al. 1996), but movement between plantings or within a region can be manipulated with an understanding of the insect s biology and some careful planning. Local movement can have a profound impact on pest management practices. As was seen with the development of resistance to spinosad in Hawaii (Zhao et al. 2002), growers essentially treated individual crucifer plantings within a field as discrete populations of P. xylostella when, in fact, the real population travelled freely between all the plantings and was continuously being selected for resistance every time one of the plantings was treated. If this field population did not also have susceptible P. xylostella immigrating into it to dilute resistant alleles, development of resistance would be further exacerbated. Likewise, it is important to understand adult movement patterns of P. xylostella to assess the potential for mating disruption using pheromones. Previous studies have shown mixed results (McLaughlin et al. 1994, Schroeder et al. 1999), perhaps not only because of the pheromone blend but also because of a lack of knowledge of adult movement patterns. Likewise, the dissemination of microbial-infected P. xylostella adults (Vickers et al. 2001) will depend on the propensity of infected adults to move and infect other adults. In a similar fashion, an understanding of movement behaviour will be essential to understand whether trap cropping can be an effective tool for arresting the movement of P. xylostella adults as they seek oviposition sites. However, it is not only the movement patterns of adult P. xylostella that should be examined, but also the movement patterns of their natural enemies (Schellhorn & Silberbauer 2002). Putting the parts together: an example from Mexico One size will not fit all, and management practices appropriate for a small farmer in Thailand may not be suitable for a large-scale grower in Australia, but each can learn something from the other. In Mexico there is a large scale P. xylostella management program that tries to implement the latest developments in technology using a landscape management approach, but it does not get much publicity since it is a commercial operation. The El Bajio region in central Mexico has been in broccoli production for over 40 years and grows up to 40,000 ha of broccoli for processing. Since much of this production is exported to the US, the quality standards are high. There are seven processors who work with the growers who supply the raw product, and these processors cooperate to a large extent because they work in the same region, often in adjacent fields, and what affects one processor will affect the others. In the late 1980s, growers in El Bajio began to have control failures because of resistance to pyrethroids and they sought advice from people who were familiar with crucifer production. The general advice was to back away from pyrethroids to allow natural enemies to exert some control, start using Bts but make sure coverage is good, sample the fields regularly and set a threshold, monitor for resistance on a regular basis and, most importantly, have a host-free period to break the life cycle of P. xylostella in that region. Generally, these recommendations were followed and the number of sprays declined by >60% in a single season without any loss in product quality. However, now growers are reporting instances of some 6 Proceedings of the 4th International Workshop, Nov. 2001, Melbourne, Australia

5 populations of P. xylostella becoming tolerant to Bt, but it is still generally effective and the situation is not nearly as bad as it was with pyrethroid resistance. As the growers and processors assess their current situation, their goals are to decrease insecticide use while maintaining or increasing the quality of the product, conserve the effectiveness of the new classes of insecticides (spinosad, emamectin benzoate and indoxacarb) and the older classes as well, enhance the use of biological control and cultural controls, and implement novel strategies if they prove effective in small trials. To achieve these goals will require something unusual in business - cooperation between companies. The seven Mexican processors can be viewed as the funnel through which the raw product flows and they must cooperate to have a regional strategy that can be followed by the individual growers. The processors must be the ones to work together to ensure that the host-free period is followed since it is the foundation for the regional management. Likewise, the processors must implement a regional resistance management program for the newer insecticides which uses a window strategy so that selection pressure for resistance to one insecticide is not constant. While they recognise the need for this (even more so now that resistance to spinosad has occurred in Hawaii), they are struggling to determine how they can do this over 40,000 ha which encompasses hundreds of different growers and for insecticides that have variable costs and efficacy. Through experience they have come to respect insecticide resistance and value the use of other tactics such as conserving natural enemies and even making augmentative releases of parasitoids. Fundamentally, they have begun to take a landscape perspective on managing P. xylostella and have initiated efforts to combine tactics and share data and knowledge more than ever before. It is too soon to determine the outcome, but it is an important program from which we can learn. The future needs of the P. xylostella research community It is important to ask what we have learned from these previous three conferences as we begin the fourth conference. One central point is that there is a wealth of information about P. xylostella and we need to communicate this knowledge within the P. xylostella research community. Secondly, nearly all of us who work in P. xylostella management have experienced control failures and these appear to have been due to one or more of the following: insecticide resistance, changing cultivation practices and the lack of effective biological control. Each of these causes may be influenced by the other. Third, management of P. xylostella will require an integrated approach since reliance on any single method is sure to fail in the long (and often short) run. Finally, it has become apparent that there is still much to be learned and that we must work as an international community so that we can develop and implement more sustainable and reliable strategies for managing P. xylostella in the future. What we don t want to see is déjà vu all over again. Acknowledgements I thank the many colleagues, past and present, whose work contributed to our present knowledge base of P. xylostella. Also thanks to N. Schellhorn for reviewing an earlier version of this paper. References Ankersmit GW DDT resistance in Plutella maculipennis (Curtis) (Lep.) in Java. Bulletin of Entomological Research 44, Chu Y The migration of the diamondback moth. In: Diamondback moth management (eds NS Talekar & TD Griggs). Proceedings of the First International Workshop, March 1985, Tainan, Taiwan, The Asian Vegetable Research and Development Center, Shanhua, Taiwan, AVRDC Publication No , pp Croft BA & Brown WA Responses of arthropod natural enemies to insecticides. Annual Review of Entomology 20, Croft BA Arthropod Biological Control Agents and Pesticides. John Wiley and Sons, New York. Diaz-Gomez O, Rodriguez JC, Shelton AM, Lagunes A & Bujanos R Susceptibility of Plutella xylostella populations in Mexico to commercial formulations of Bacillus thuringiensis. Journal of Economic Entomology 93, Dosdall LM, Mason PG, Olfert O, Kaminski L & Keddie BA The present and future status of diamondback moth, Plutella xylostella (L.) as pest of canola in western Canada (Abstract). In: The management of diamondback moth and other crucifer pests (eds NM Endersby & PM Ridland): Proceedings of the Fourth International Workshop, November 2001, Melbourne, Victoria, Australia (this volume). Food and Agriculture Organization of the United Nations (FAO) Agriculture data. Georghiou GP & Lagunes-Tejeda A The Occurrence of Resistance to Pesticides in Arthropods. Rome: Food and Agriculture Organization. Proceedings of the 4th International Workshop, Nov. 2001, Melbourne, Australia 7

6 Gupta PD & Thorsteinson AJ Food plant relationship of diamondback moth (Plutella maculipennis (Curt.)). I. Gustation and olfaction in relation to botanical specificity of larvae. Entomologia Experimentalis et Applicata 3, Harcourt DG Population dynamics of the diamondback moth in southern Ontario. In: Diamondback moth management (eds NS Talekar & TD Griggs). Proceedings of the First International Workshop, March 1985, Tainan, Taiwan, The Asian Vegetable Research and Development Center, Shanhua, Taiwan, AVRDC Publication No , pp Hillyer RJ & Thorsteinson AJ The influence of the host plants or males on ovarian development or oviposition in diamondback moth, Plutella maculipennis (Curt.). Canadian Journal of Zoology 47, Hu YER, Mitchell D, Sieglaff H & Okine JS Field production of two species of parasitoids of the diamondback moth (Lepidoptera: Plutellidae). Florida Entomologist 81, Javier EQ Foreword. In: Diamondback moth and other crucifer pests (ed NS Talekar). Proceedings of the Second International Workshop, Tainan, Taiwan, December 1990, Asian Vegetable Research and Development Center, Shanhua, Taiwan, AVRDC Publication No , p. 11. Johnson DR Plutella maculipennis resistance to DDT in Java. Journal of Economic Entomology 46, 176. Lasota JA & Kok LT Diadegma insulare (Hymenoptera: Ichneumonidae) parasitism of the diamondback moth (Lepidoptera: Plutellidae) in south Virginia, U.S.A. Journal of Entomological Science 21, McLaughlin JR, Mitchell ER & Kirsch PA Mating disruption of diamondback moth (Lepidoptera: Plutellidae) in cabbage: Reduction of mating and suppression of larval populations. Journal of Economic Entomology 87, Schellhorn NA & Silberbauer LX The role of crops and surrounding vegetation: increasing the effectiveness of predators and parasitoids in cotton and broccoli systems. First international symposium on biological control of arthropods. Program and Abstracts. Honolulu, Hawaii. Schroeder PC, Shelton AM, Ferguson CS, Hoffmann M & Petzoldt C Application of synthetic sex pheromone for management of diamondback moth, Plutella xylostella, in cabbage in New York. Entomologia Experimentalis et Applicata 94, Shelton AM, Kroening MK, Eigenbrode SD, Petzoldt C, Hoffmann MP, Wyman JA, Wilsey WT, Cooley RJ & Pedersen LH Diamondback moth (Lepidoptera: Plutellidae) contamination of southern-grown cabbage transplants and the potential for insecticide resistance problems. Journal of Entomological Science 31, Shelton AM, Sances FV, Hawley J, Tang JD, Bourne M, Jungers D, Collins HL & Farias J Assessment of insecticide resistance after the outbreak of diamondback moth in California in Journal of Economic Entomology 93, Shelton AM & Roush RT Resistance to insect pathogens and strategies to manage resistance. In: Field Manual of Techniques in Invertebrate Pathology (eds LA Lacey & HK Kaya). Kluwer Academic Press, pp Shelton AM International Working Group for Diamondback Moth. Shelton AM, Wilsey WT, Hoebeke ER & Schmaedick MA Parasitoids of cabbage Lepidoptera in Central New York. Journal of Entomological Science 37, Talekar NT & Shelton AM Biology, ecology and management of the diamondback moth. Annual Review of Entomology 38, Van Driesche RG & Bellows TS Biological Control. Chapman and Hall, New York. Vickers RA, Pell JK, White A & Furlong MJ Proof-of-concept trials for control of DBM by auto-dissemination (Abstract). Fourth international workshop on the management of diamondback moth and other crucifer pests. Program and Abstracts. Melbourne, Australia. Xu J, Shelton AM & Cheng X Variation in susceptibility of Diadegma insulare to permethrin. Journal of Economic Entomology 94, Zhao JZ, Wu S, Gu Y, Zhu G & Ju Z Strategy of insecticide resistance management in the diamondback moth. Scientia Agricultura Sinica 29, Zhao JZ, Li Y, Collins HL, Gusukuma-Minuto L, Mau RFL, Thompson GD & Shelton AM Monitoring and characterization of diamondback moth resistance to spinosad. Journal of Economic Entomology 95, Proceedings of the 4th International Workshop, Nov. 2001, Melbourne, Australia

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