Published online 26 March 2009
Techniques for the treatment, removal and disposal of host material during programmes for plant pathogen eradication
Version of Record online: 26 MAR 2009
© 2009 The Authors. Journal compilation © 2009 BSPP
Volume 58, Issue 4, pages 621–635, August 2009
How to Cite
Sosnowski, M. R., Fletcher, J. D., Daly, A. M., Rodoni, B. C. and Viljanen-Rollinson, S. L. H. (2009), Techniques for the treatment, removal and disposal of host material during programmes for plant pathogen eradication. Plant Pathology, 58: 621–635. doi: 10.1111/j.1365-3059.2009.02042.x
- Issue online: 20 JUL 2009
- Version of Record online: 26 MAR 2009
- disease detection;
- Top of page
- Eradication case studies
- Techniques for eradication and containment of plant pathogens
Eradication of plant pathogen incursions is very important for the protection of plant industries, managed gardens and natural environments worldwide. The consequence of a pathogen becoming endemic can be serious, in some cases having an impact on the national economy. The current strategy for eradication of a pathogen relies on techniques for the treatment, removal and disposal of affected host plants. There are many examples where these techniques have been successful but many where they have not. Success relies on a sound understanding of the biology and epidemiology of the pathogen and its interaction with the host. Removal and disposal of infected plant material for eradication and containment of plant and soil inhabiting fungal, bacterial and viral pathogens are reviewed by considering black Sigatoka of banana, apple scab, maize smut, fireblight, citrus canker and sharka disease of stone-fruit crops. In examining examples of dealing with plant pathogens and diseased host material around the world, particularly Australasia, various techniques including burning, burying, pruning, composting, soil- and biofumigation, solarization, steam sterilization and biological vector control are discussed. Gaps in the literature are identified and emphasize the insufficient detail of information available from past eradications. More effort is required to produce and publish scientific evidence to support the success or otherwise of techniques and suggestions for future research are proposed.
- Top of page
- Eradication case studies
- Techniques for eradication and containment of plant pathogens
An incursion is defined as an isolated population of a pest recently detected in an area, not known to be established, but expected to survive for the immediate future (Anon, 2007) and can threaten the economic viability of plant industries worldwide. The isolation of island nations such as Australia and New Zealand has assisted in the exclusion of many plant pathogens endemic in other parts of the world. In Australia, the farm-gate value of plant industries is over A$15 billion and contributes over A$10 billion to export income (The Australian Bureau of Agricultural and Resource Economics, ABARE). In New Zealand farm gate value of plant industries is approximately NZ$11 billion with export incomes of around NZ$7 billion (Statistics New Zealand). Eradication is defined as the elimination of a pest from an area using phytosanitary measures (Anon, 2007). Eradication programmes can be expensive, requiring a great deal of labour and resources, but often provide great economic benefit. The recent eradication of citrus canker from Queensland cost approximately A$18.5 million. However, this cost was regarded as affordable in order to give long-term benefit and preserve the A$105 million citrus industry in Australia (ABARE; Telford, 2007). In Florida, USA, the cost of citrus canker eradication between 1995 and 2005 was estimated at nearly US$1 billion (Gottwald & Irey, 2007). The eradication of fire blight from Melbourne Royal Botanic Gardens in 1997 cost approximately A$20 million, but this too may have prevented Australian pome fruit industry losses of up to A$870 million had the disease become endemic (Rodoni et al., 2006). Murray & Brennan (1998) estimated potential annual losses of A$491 million should Karnal bunt of wheat become endemic in Australia, based on losses in yield, quality and export markets as well as costs of control seed production and research. Predictive costs of an outbreak of Karnal bunt in the European Union have recently been presented (Sansford et al., 2008). The eradication of black Sigatoka from the Tully Valley in Queensland in 2001–3 cost A$17 million (A. Daly, unpublished data). However, the increased cost to the industry in Tully of not eradicating the pathogen, borne from increased de-leafing and chemical application, would have been nearly A$90 million over a 5-year period. In 2006, Cyclone Larry destroyed much of the banana crop in Innisfail, the largest single banana production area of northern Queensland. Queensland production accounts for 95% of bananas entering Australia's central markets. The massive crop loss caused the consumer price index to jump, the price of bananas rising ten-fold. A similar crop loss and resulting impact on the industry and the Australian economy could be experienced should a wide-scale outbreak of an exotic pathogen occur in Australia's relatively small banana production area.
An exotic plant pathogen can be detected in imported material (interception) or as a replicating population following a field outbreak. Ebbels (2003) suggested that the action taken in response to an interception of imported material is often short-term as it is isolated, whereas a field incursion or outbreak detected as a replicating population requires a longer-term approach. The management of an incursion has three alternative responses: eradication, containment or no action. Containment is defined as the application of phytosanitary measures in and around an infested area to prevent spread of a pest (Anon, 2007). The response taken will often depend on the net economic benefit (Fraser et al., 2006). Eradication is likely to be attempted where export markets will be affected and success of the eradication is probable. Sometimes the only option may be to contain or limit spread or, in some cases, do nothing at all despite the potential loss of export markets. Many pathogens are subject to phytosanitary requirements on interceptions and outbreaks or movement of plant material in existing legislation and through the International Plant Protection Convention. According to Simberloff (2003), the success of eradication depends on adequate resources, a commitment to see the programme through to completion, establishment of clear lines of authority, the target species to be detectable at low densities and subsequent intensive management of the system.
The current strategy for eradication of an exotic plant pathogen outbreak involves the following general steps: (i) surveillance to locate source and extent of the infection, (ii) removal of infected and potentially infected plant material, (iii) disposal of plant material (e.g. burn and/or bury), (iv) quarantine and movement controls to prevent the spread of the pathogen, and (v) surveillance to confirm freedom from pathogen. Due to the broad scope of eradications, this review focuses mainly on steps (ii) and (iii), areas requiring more research. Several case studies of eradication or containment of plant and soil inhabiting fungal, bacterial and viral pathogens of both perennial and annual crops are presented. Examples are predominantly taken from Australasia but also draw from cases further abroad. An integrated approach is often employed to contain or eradicate a plant pathogen. Methods for removal and disposal are then evaluated, drawing on information from these and other eradication and control programmes reported worldwide. The objective is to provide information which may lead to the optimization of existing methods or the development of novel eradication methods.
Eradication case studies
- Top of page
- Eradication case studies
- Techniques for eradication and containment of plant pathogens
Black Sigatoka of banana
Black Sigatoka (black leaf streak) is a disease of banana (Musa spp.) caused by the ascomycete fungus Mycosphaerella fijiensis and is endemic in many parts of the world (Mulder & Holliday, 1974). The pathogen produces conidia and ascospores on leaf lesions which are spread by rain and wind to infect new banana leaves. Australia remains free of black Sigatoka despite several outbreaks which have occurred in commercial production areas. Jones (1984) reported the first attempt to eradicate black Sigatoka from the Australian mainland and three neighbouring islands following its detection in the northern Cape York Peninsula and the Torres Straight region in 1981. The campaign involved injection of banana plants with herbicide (glyphosate) to kill all bananas in the infested areas. Most leaf and pseudostem residues were destroyed later by burning. Re-planting bananas in the eradication areas was not permitted for 6 months during the wet summer when break-down of remaining plant residues was accelerated. The decision for this host free period was based on data from previous research on the longevity of M. musicola (Stover, 1980), the cause of yellow Sigatoka of banana. Conidia, ascospores and perithecia of M. musicola did not remain viable on detached banana tissue for longer than 3 to 4 months. Despite these attempts, black Sigatoka reappeared in the northern Cape York Peninsula and on Thursday Island in 1984. This may have been due to survival of the pathogen on banana residue for longer than expected, the failure to locate all stands of bananas near infested areas, or re-introduction of the pathogen via airborne spores or with planting material or leaves from other nearby infested areas north of the mainland (Jones, 1984).
Peterson et al. (2005) reported that between 1981 and 2000, black Sigatoka was detected in a further six locations in Cape York Peninsula, most likely resulting from introductions of infected planting material from the Torres Strait region. The outbreaks were eradicated on each occasion using different methods to destroy the infected plants (Peterson, 2002). These included injection with herbicide, removal of plants followed by burial and burning or disc ploughing of felled plants. Resistant cultivars were supplied for re-planting in most cases.
The disease was detected again in 2001 in the Tully area, the major banana-growing region of Australia. A programme of intensive de-leafing was employed to remove the majority of inoculum from plants (Peterson et al., 2005). Leaves removed from plants were placed on top of one another on the ground to reduce ascospore release, a strategy shown to be effective for M. musicola (Peterson et al., 2000). Two months later, leaf material was inspected microscopically and M. fijiensis was not detected. To prevent establishment of new infections, mancozeb, propiconazole, difenoconazole, tebuconazole and trifloxystrobin fungicides mixed with mineral oil were applied to plants weekly in rotation for 6 months. Organic growers applied copper-based fungicides plus vegetable oil in rotation with mineral oil alone. The presence of remaining inoculum was monitored using transects of sentinel plants not subjected to fungicides. No further inoculum was detected. Temperature and rainfall data were also analysed to indicate the number of disease cycles that would have occurred during the 6-month period. A statistical model was developed to simulate the multiplication and spread of the pathogen and provided a very high level of confidence that the pathogen had been eradicated (Peterson et al., 2005). The success of the Tully eradication programme was attributed in part to early disease detection, the approaching dry season (suppression of ascospore production) and the biology of the fungus (no alternative hosts and long-term survival structures).
Apple scab, caused by the ascomycete fungus Venturia inaequalis, overwinters as pseudothecia in infected leaves on the ground, and ascospores, the primary source of inoculum, are spread by rain and wind to infect new leaves and fruit (MacHardy, 1996). Conidia are then formed and provide secondary infection of more leaves and fruit throughout the season. Apple scab was the subject of several eradication programmes in Western Australia between 1930 and 1996, and since then this Australian state is currently the only apple-producing region in the world free of the disease (MacHardy, 1996; McKirdy et al., 2001). In 1930 apple scab was confirmed in several apple orchards, leading to an eradication programme which involved boiling all apples removed from trees and the orchard floor, application of Bordeaux fungicide and cultivation of the orchard floor (Pittman, 1936). In 1936, introduction of V. inaequalis on nursery stock from Victoria prompted eradication measures similar to that in 1930 (Pittman, 1936; Cass Smith, 1940). In addition, all imported nursery stock was dipped in Bordeaux fungicide and the entry of all pome fruit into Western Australia was prohibited. Further outbreaks in 1940 were again subjected to intensive eradication efforts and reported to be successful when the disease was not detected during inspections over the following 5 years (Cass Smith, 1940; Powell & Cass Smith, 1944). In 1947–48, apple scab was detected in orchards and nurseries and subsequently traced back to nursery stock imported from Victoria and Tasmania (Cass Smith et al., 1948). Eradication measures included the complete destruction of all trees with apple scab and the cutting back to basal dormant buds of any adjacent symptomless plants, although details of the methods of destruction were not available. The disease was not detected in Western Australia for a further 40 years.
Between 1989 and 1996, several new outbreaks of apple scab occurred and intensive eradication programmes followed: strategies were developed to interrupt the lifecycle of the fungus (Cripps & Doepel, 1993). Initially, compulsory spraying with the fungicide Baycor 300 (bitertanol) was conducted after harvest and before leaf fall. At 20% leaf fall, 5% urea solution was applied to reduce pseudothecium formation. After leaf fall the whole orchard floor was sprayed with 5% urea to assist microbial break-down of leaf litter. Leaves were manually raked into rows and mulched using a flail mower. Neglected orchards were removed, all leaf litter treated as above and trees burnt.
Apple scab has not been detected in Western Australia since 1996 and the success of the eradication measures has been attributed to containment of new outbreaks, preventing spread within and between districts, disrupting the lifecycle of the fungus during winter, and preventing infection and disease by applying flusilazole fungicide in the spring-early summer period (Doepel, 1997; McKirdy et al., 2001).
Common smut of maize
Common smut (Ustilago maydis) is a basidiomycete fungal disease of maize which survives for up to several years as teliospores in soil or on crop debris. In the presence of moisture in spring or summer, teliospores germinate to form basidia (promycelia) which produce basidiospores. Basidiospores are spread by rain and wind to infect developing plant tissue, eventually forming galls in which new teliospores develop. These either reinfect young plants or overwinter in soil or debris. Ustilago maydis was first detected on North Island, New Zealand in a crop at Gisborne in 2006. A survey of the area revealed that smut-affected plants were concentrated in five rows of one crop (Froud et al., 2006). Plants with immature galls were immediately removed, placed into double-layered plastic bags and then incinerated. Four to five medium-sized galls had erupted to various degrees before they could be removed. Soil beneath the infected plants was collected into double bags and incinerated. Plants remaining in the affected crop were mechanically cut into 2–3 pieces using a special harvester causing minimal disturbance. Plants from the affected area of the field were placed at the bottom of a compost heap on black polythene while those from the remainder of the crop around the affected plants (buffer zone) were placed in the centre of the heap. The remainder of the crop with no galls was placed on top and then the entire heap was covered with plastic sheeting and car tyres. Solarization treatment of soil beneath the affected crop was undertaken by securing plastic sheeting over the affected site through spring–summer 2006–7 (Gill, 2008; G. Gill, personal communication). A survey confirmed no further disease was present in the region (Froud et al., 2006) although the presence of U. maydis was not assessed following incineration, ensilage or solarization processes. Thus far, the eradication programme was not complete, but all indications were that the fungus had been eradicated. While no soil testing is planned, a restriction on growing maize at the site exists and will be reviewed in 2009 (G. Gill; M. Bullians, personal communication).
Fire blight of apple and pear
Fire blight, caused by the bacterium Erwinia amylovora, is a disease of pear and apple and several ornamental plants in Rosaceae (Hayward & Waterson, 1965). The pathogen overwinters as wood cankers and is spread primarily by bees, flies, ants and rain splash to infect blossoms followed by subsequent infections in shoots, leaves and fruit by rain splash and insects. In parts of northern Europe such as UK and Denmark, the pathogen overwinters in Crataegus spp. (Billing et al., 1974). It occurs in 43 countries of North America, Europe, Asia and Africa including New Zealand, although Australia remains free of the disease. Erwinia amylovora was found on two trees (Cotoneaster and Sorbus) in the Melbourne Royal Botanic Gardens (RBG) in 1997 (Jock et al., 2000). This led to the initiation of an eradication programme (Rodoni et al., 1999) which involved the removal of 685 individual host plants (viz. Pyrus, Malus, Cotoneaster, Crataegus, Pyracantha and Sorbus) within 250 m of the RBG boundary and the removal of 34 feral bee colonies from within 1000 m. Strict quarantine protocols were used for the removal of the plants, and involved the use of disposable clothing and digging the entire plants out of the ground then wrapping them in plastic to avoid plant to plant contamination. Foliage and wood was placed in sealed bags and buried 2 m deep at a site located 30 km from the RBG (Rodoni et al., 1999). The remaining stumps were ground out and the areas from where the plants were removed were steam fumigated. National surveys in the three years following the incursion of E. amylovora in the RBG did not detect the disease or the fire blight pathogen (Rodoni et al., 2002).
An incursion of fire blight in Norway occurred in the city of Stavanger, on the south west coast, in 1986 (Sletten, 1990). Diseased plants were found in private gardens, around public buildings, in recreation gardens and along roadsides on species of Cotoneaster, Sorbus and Pyracantha. The nearest commercial apple and pear fruit district was located about 40 km north of the incursion site. The aim of the subsequent eradication programme was to protect the nurseries within the city and prevent the spread of the disease into the commercial production area. A quarantine area of around 700 km2 was established around the focus of the infection and diseased plants and susceptible hosts were removed, although the number of trees removed was not indicated (Sletten, 1993). Within the quarantine area, the production and sale of all common fire blight hosts was prohibited. More than 60 000 private gardens were checked, in addition to public gardens and roadsides. A mobile wood chipper was used to mulch plant material into fine chips, which were then decomposed in compost heaps for at least one year (Sletten & Melboe, 2004), but no further detail was provided. Bee hives were moved to areas that were free from hosts of E. amylovora. Fire blight was detected at around 2000 locations in the quarantine area during the years 1986–1992 although from 1990 there was a significant decline in new outbreaks (Sletten, 1993). The systematic surveillance of the quarantine zone continued every year until 1998 and was expanded to include other areas in Norway. The removal of the main hosts of fire blight greatly reduced the build up of inoculum and also simplified annual surveillance of the disease. It was assumed that the lack of optimal climatic conditions for the pathogen, particularly during spring, may have helped restrict the spread of the disease. Fire blight was not detected in Norway between 1993 and 2000 (Sletten & Melboe, 2004). It is not clear if the recent detection of fire blight within the restriction zone in 2000 is due to the re-emergence of the original inoculum or a more recent introduction. Although no evidence was provided, it was believed that the limited spread from this incursion was due to the illegal movement of contaminated Cotoneaster plants and beehives between private gardens. The strict eradication campaign has now been re-established in Norway to prevent the spread of fire blight into the important fruit growing areas and nurseries (Sletten & Melboe, 2004).
Fire blight was first reported in Israel in 1985 and within 10 years posed a serious threat to the national pear industry due to the emergence of streptomycin-resistant strains of E. amylovora through its routine use for management of fire blight during this period. Although fire blight has not been eradicated, control has been achieved with a management programme called Fire-Man (Shtienberg et al., 2002). Fire-Man aims to reduce the amount of inoculum in the orchards before bloom, protect blossoms from infection and sanitation of infected plant tissues after bloom. Infected tissue was removed by pruning out blighted branches and limbs 30 cm below the margin of the canker (Shtienberg et al., 2002). An alternative method of removing inoculum involved in situ burning of blighted tissues by applying a propane torch directly to the pear trees (Reuvini et al., 1999). However, Shtienberg et al. (2002) reported that it had no effect on internal populations of E. amylovora and the heat created wounds on surviving limbs, increasing chances of reinfection. The Fire Blight Control Advisory system (FBCA) (Shtienberg et al., 1999) uses thresholds of temperature and leaf wetness based on local experience and this proved to be the best fire blight prediction model in Israel compared to ‘Maryblyt (Shtienberg et al., 2002). The initial strategies in Israel were aimed at containment and eradication of E. amylovora, but since the mid nineties there has been a shift towards intensive management practices to protect the national pear industry from severe losses caused by fire blight. In the USA, fire blight prediction models such as ‘Maryblyt’ (Steiner, 1990) or ‘Cougarblight 98C’ (Smith, 1999) have been developed based on temperature and leaf wetness, and are used for the timely application of chemicals to control the disease.
Fire blight became established in the Emilia-Romagna region of Italy in 1997 following failure of measures which included destruction of 500 000 pear trees (Calzolari et al., 1999). Short distance spread of E. amylovora from undetected infection foci within the region and the long distance spread of greater than 14 km from neighbouring districts by birds were cited as the source of inoculum (Battilani et al., 1999). These examples demonstrate the difficulty of eradicating fire blight and in some cases containment or control may be the only option. In the European Union, ‘protected zones’ have been established for E. amylovora, preventing further spread by movement of host plant material and bees into countries and areas free of the pathogen (Anon, 2003).
Citrus canker, caused by the bacterium Xanthomonas smithii subsp. citri, formerly X. campestris pv. citri or X. axonopodis pv. citri (Schaad et al., 2005) has been found in most continents of the world except Europe. The pathogen has been eradicated in South Africa, Australia, Fiji, Mozambique and New Zealand (Schubert et al., 2001) and eradication programmes are continuing in Argentina, Uruguay and Brazil but have been started and stopped in Florida, USA. Xanthomonas smithii forms canker lesions on fruit, leaves and twigs of citrus plants and upon wetting, bacteria multiply and ooze to the surface (Gottwald et al., 2001). Wind driven rain can spread the bacteria up to 15 km from the source to infect citrus trees via stomata or wounds.
Citrus canker was detected on lemon (Citrus limon), orange (C. sinensis) and other Citrus spp. in Kerikeri, North Island, New Zealand in 1937 and subsequently on most of the North Island (Reid, 1938). Removal of lateral branches and all green tissue such as leaves, petioles and thorns were removed from affected lemon, orange, grapefruit and citronella trees then sprayed with polysulphide chemicals (0.2% lime sulphur) and wounds treated with bitumen paint or petrolatum. Excised plant material was burned and leaf material remaining on the orchard floor was ploughed in. All citrus trees in affected orchards were treated and, citrus trees with old, infected wood in private gardens were removed and burned. The eradication was largely successful, but the disease appeared in Auckland in 1960 (Dye, 1960) and again in Taranaki (350 km south of Auckland) in 1972 (Pennycook et al., 1989). Citrus canker was again eradicated using methods similar to those described above. Surveys continued until 1993, when New Zealand was declared to be free of citrus canker (Taylor et al., 2002).
In Australia, citrus canker was detected on Thursday Island in Queensland, and an eradication campaign was initiated in 1984 (Jones et al., 1984). Ten citrus trees with symptoms, including lime (C. aurantifolia) and orange, were destroyed by lopping and incineration, along with any citrus within 15 m of infected trees. Vegetation under the canopies was burnt to ground level using a flame gun and herbicide applied to citrus stumps to prevent regrowth. Replanting and movement of citrus material was restricted. Surveys led to several detections near the original outbreak up until 1986, however continued monitoring for the following 2 years failed to detect citrus canker, and Thursday Island was declared to be free from the disease in 1988 (Jones, 1991).
In 2004 an outbreak of citrus canker in Emerald, Queensland prompted an eradication programme which involved removal and disposal of infected and suspect plant material, strict quarantine controls and regular surveillance (Telford, 2007). Destruction of 495 000 commercial citrus trees and 4300 residential or ornamental citrus trees was carried out by bulldozing the trees into heaps and burning. An 18-month ‘host-free’ period (concluded in June 2007) in the quarantine area was undertaken. Xanthomonas smithii subsp. citri was not detected in a study of potential reservoirs on residual plant material in the soil (Gambley et al., 2007). Continued surveillance every 3 months until December 2008 will determine the success of the eradication.
In the Northern Territory, Australia, citrus canker has been detected and successfully eradicated on two occasions. In 1912, severe disease was observed in limes and lemons at Stapleton (110 km south of Darwin) and on most citrus trees within the vicinity of Darwin. All citrus trees and stock at the Botanic Gardens and the affected trees at Stapleton were destroyed by fire. Movement of citrus trees and fruits out of the Northern Territory was prohibited (Hill, 1918). Further detections of citrus canker in 1918 and then in 1922 led to the decision to destroy all citrus north of latitude 19°S. A successful eradication was achieved by removing and burning trees with quarantine restrictions lifted in 1924 (Mertin, 1952). In 1991 citrus canker was again detected in the Northern Territory on pummelo (C. maxima) trees in an orchard in Humpty Doo, 50 km south-east of Darwin. The property and surrounding area were placed under quarantine and trees on the affected property were burned in situ (Broadbent et al., 1995). A further outbreak was detected in 1993 on another property 500 m from the first and was concluded to have originated from the previous outbreak (Broadbent et al., 1995). All citrus on this and adjoining properties was destroyed, creating a 400 m buffer zone around the two infection sites. Eradication was declared successful in 1995 (Pitkethley & Ulyatt, 1995).
Citrus canker was first found widespread in Florida, USA in 1912 and eradicated by 1933 through regular nursery and orchard inspection, on-site destruction of infected trees and nursery plants by burning, good sanitary practices by citrus workers and enforcement of strict quarantines (Schoulties et al., 1987). In 1984 an outbreak arose in a nursery in Polk County and following extensive surveys, 20 million young citrus trees were removed and burned (Schoulties et al., 1987). In 1986, citrus canker was found in residential and commercial citrus trees in the Tampa Bay area (Schubert et al., 2001). Eradication was declared in 1994 and was achieved by removing and burning all citrus trees within 38 m of infected trees. In 1995, citrus canker was detected in residential trees in Miami and then further detections were made in commercial orchards in Manatee County (Graham et al., 2004). The eradication campaign involved removal of all citrus within 579 m of infected trees by chainsaw followed by wood chipping and transport in a covered trailer to a landfill. It was found that some debris infected with X. smithii escaped during transport and dumping and have potential to cause re-infection (Graham et al., 2004). Following Hurricane Wilma in 2005, citrus canker spread widely and was declared endemic in Florida and eradication was discontinued (Gottwald & Irey, 2007). Efforts are now concentrated on best management practices for citrus canker and minimizing production losses.
Belasque et al. (2005) describe two experiments for the eradication of citrus canker in Brazil. In the first, all diseased plants in five orchards were removed and, when two or more diseased plants were adjacent, the plants within a 30 m radius of the diseased plants were drastically pruned. In the second experiment, diseased plants in 12 orchards were similarly pruned including plants within a 30 m radius of the diseased plants. The drastic pruning protocol consisted of removing all branches, leaves and fruit, including any plant material on the ground, followed by burning and burial on site. The remaining trunks were painted with lime and copper oxychloride. All citrus trees in a 2 km radius of experimental orchards were inspected every 3 months and any plants showing symptoms eliminated. Citrus canker affected plants were found 8–11 months after pruning in six orchards, one in the first experiment and five in the second. In the other 11 orchards, no plants expressing symptoms were found in 2 years of monitoring. It was concluded that drastic pruning could be applied as an effective method of control of citrus canker, but not for complete eradication.
Sharka disease of stone fruit
Sharka disease, caused by Plum pox virus (PPV), is one of the most serious viral diseases of stone-fruit crops (Prunus spp.) and occurs throughout Europe, the Middle East, Africa and South America (Brunt et al., 1996). The virus is spread by vegetative propagation, aphid vectors and seed.
PPV was first detected in North America in 1999 in Pennsylvania in peaches (P. persica) (Levy et al., 2000). The PPV incursion was confined to several counties in Pennsylvania due to a national surveillance programme and aggressive eradication measures (Hughes et al., 2002). The latter involved removing all trees within a production block where a PPV-infected tree had been detected plus all trees within a 500 m radius of the infected tree, resulting in the removal of 650 hectares of commercial orchards. Targeted surveys conducted in Pennsylvania from 2003–2005 on over one million commercial nursery and residential trees showed that the incidence of PPV detection in these areas had declined significantly (Levy, 2006).
Monitoring and eradication of PPV involved the removal of infected trees from plum (P. domestica) and apricot (P. armeniaca) orchards over a 15-year period in the Puglia region of Italy, where it was found in the province of Lecce (Myrta et al., 2006). The programme supported by decree of mandatory control involved annual monitoring of orchards and nurseries by visual observation, leaf sampling and testing. Orchards with more than 30% of trees infected were completely removed, including roots. No orchards exhibited 10–30% infection, and when infection did not exceed 10%, removal was limited to infected and adjacent trees. All trees removed were burned (A. Myrta, personal communication). Continued surveillance since 1994 indicates that the Puglia region is now free of PPV and the use of certified virus-tested plants is advised by the regional phytosanitary service together with the collaboration from stone fruit nurserymen.
PPV was discovered in stone fruit orchards in Ontario and Nova Scotia, Canada in 2000 (Thompson, 2006). Individual trees were tested for PPV and only infected trees were removed, unless the incidence of PPV in a block was greater than 10%, in which case the entire block was removed. However, Thompson (2006) did not report the means of disposal of plant material. Over time the threshold value has been lowered to 1.5% and a certification scheme has been designed to provide clean replacement trees, in the hope that PPV will be eliminated from Canada by 2010.
In 1996, PPV was detected in plum trees in the Netherlands (Verhoeven et al., 1998). All infected trees (cv. Jubileum) had been imported from elsewhere in the European Union since 1994. All orchards planted with material of this origin in the Netherlands were surveyed using visual diagnosis and enzyme-linked immunosorbent assay (ELISA). Fourteen percent of all trees were infected in 29 of 43 orchards. Inspection of the 12 500 plum trees remaining in these orchards revealed 13 infected trees of five other cultivars. All infected trees were removed and burned during the autumn and winter of 1996–97 (Verhoeven et al., 1998; J. Verhoeven, personal communication). The planting of certified virus-free propagation material, followed by inspections in nurseries and orchards, and large scale ELISA testing for PPV also contribute to the limited occurrence of up to just 50 plants per year with PPV in the Netherlands at present (Verhoeven et al., 2008).
Although discovered in 1961 an eradication programme for PPV in Poland was begun in 1996. This programme included elimination of PPV from nursery material and commercial orchards as well as from other potential hosts, especially in the areas surrounding nurseries (Zandarski & Zych, 2005). Infected trees were removed and propagation from affected orchards was prohibited until declared free from the virus. Aphid control was achieved using insecticide sprays. Although eradication was not completely successful, Zandarski & Zych (2005) reported that PPV was almost eradicated from nurseries and orchards and the movement of the infected plant material has virtually ceased.
Techniques for eradication and containment of plant pathogens
- Top of page
- Eradication case studies
- Techniques for eradication and containment of plant pathogens
The case studies described above are generally well documented and demonstrate the integration of numerous techniques for eradication and containment of plant pathogens. There are many other examples of eradication, containment and control of plant pathogens of which specific techniques are discussed below.
Burning is often the preferred method of disposal as it eliminates the affected material and immediately kills any pathogens it may contain, according to Ebbels (2003). However, there are numerous examples where burning has reduced incidence or contained pathogens, but not eradicated them. Burning has been used in both successful and unsuccessful eradication programmes already described but testing for viable pathogens in ash and debris remaining after burning has not been reported. Similarly, the temperature and duration of burning are rarely documented. Temperature may be important in pathogen mortality, as was shown in a study in which rice stubble was burnt in an attempt to eradicate sheath diseases of rice caused by Rhizoctonia oryzae and R. oryzae-sativae in New South Wales, Australia (Lanoiselet et al., 2005). Whilst the amount of inoculum was reduced, the variable temperatures and duration of heat exposure within the rice straw may not have killed all of the sclerotia of R. oryzae. A subsequent experiment revealed that a temperature above 107°C for at least 90 s was required for 100% mortality of sclerotia (Lanoiselet et al., 2005).
Burning of crop residue has been an effective means of controlling fungal pathogens, most often in combination with other methods such as chemical tillage or crop rotation, and has been used to control fusarium disease in wheat and sorghum (Burgess et al., 1996), eyespot (Boer et al., 1993) and Karnal bunt in wheat (Singh et al., 1993) and ascochyta blight in chickpea (Gan et al., 2006). In the case of Karnal bunt, unpublished data has also been reported on the collection of T. indica teliospores in aerial samples above burning wheat stubble as well as insufficient temperatures to kill spores at the soil surface (Sansford et al., 2004). In a review by Hardison (1976), control of plant disease by ‘thermosanitation’ through application of fire and/or flame indicated a number of cases where burning had reduced the incidence of plant pathogens. Examples included brown spot needle blight (Scirrha acicola) and fusiform rust (Cronartium fusiforme) in pine trees; apple scab (V. inaequalis); dieback (Diaporthe vaccinii) and canker (Godronia cassandrae) of blueberries; flag smut (Urocystis agropyri), stem eyespot or foot rot (Pseudocercosporella), root rot or take-all (Gaeumannomyces) of wheat; scald (Rhynchosporium secalis) and net blotch (Pyrenophora teres) of barley; Septoria avenae on oats and brown spot (Pleiochaeta setosa) of lupin. In the USA, ergot (Claviceps purpurea) and blind seed disease (Gloeotinia temulenta) were effectively controlled in grass seed crops by burning stubble (Hardison, 1980). In the case of ergot, fire destroyed most of the sclerotia in crop residues and on the soil surface. In an attempt to eradicate Moniliophthora (Crinipellis) perniciosa on cocoa in Brazil, removal and burning of trees resulted in containment of witches’ broom disease to the state of Bahia, Brazil (Pereira et al., 1996). Powdery mildew (Erysiphe flexuosa) of horse chestnut was controlled in Poland by burning fallen leaves and fruit to limit the spread of spores (Adamska et al., 2002). Control of fusarium wilt of bananas (Fusarium oxysporum f.sp. cubense) was achieved in China by removing and burning infected plants, and spraying the soil with the fungicide triadimefon three times at 25-day intervals (Lin, 2004). No information on the temperature or duration of burns in any of these examples was provided. Walduck & Daly (2007) conducted field experiments in Australia to monitor the effect of burning on heat penetration through the soil profile and the ability to eliminate inoculum of the ‘Tropical’ race 4 strain of F. oxysporum f.sp. cubense, the cause of banana fusarium wilt within the soil and buried pieces of infected banana tissue. Separate laboratory experiments had shown that temperatures of 65ºC and 90ºC were necessary to eliminate microconidia and chlamydospores, respectively. Temperature recordings showed that heat did not reliably penetrate the soil below 200 mm at the temperature required to kill the pathogen in banana residue. This was confirmed by isolations from the buried tissue. Temperatures at just 10 cm below the surface were not high enough to eliminate the chlamydospores. Lateral transfer of heat within the profile was also minimal.
Control of bacterial diseases has also been achieved using management programmes which involve burning of infected plant material. Examples include bacterial leaf spot of strawberry (Xanthomonas fragariae) in Belgium (Lieten, 1998) and a number of diseases of cucumber, melon and squash caused by species of Pseudomonas, Xanthomonas and Agrobacterium in Brazil (Oliveira & Moura, 1994). Again, information on temperature and duration of burning was not provided.
Burying infected plant material is appropriate in cases where burning is not practical, such as large volumes of potatoes or root vegetables (Ebbels, 2003). Burial of both burned and unburned plant material has been used extensively in disposal of infected material as part of the eradication of plant pathogens, as described earlier. This method was employed as part of the successful eradication of fire blight from Australia. However, in the unsuccessful eradication of citrus canker in Florida, escape of debris during transport to the burial site may have compromised the programme. Ebbels (2003) highlights the importance of preventing the escape of pathogens using sealable containers or impermeable covers on high-sided trucks in transit. An incursion of grapevine leaf rust (Phakopsora euvitis) in the urban area of Darwin in the Northern Territory of Australia in 2001 (Weinert et al., 2003) led to an eradication programme which involved cutting diseased vines at ground level, applying herbicide to the stump to prevent regrowth, and disposal of excised material by deep burial (West, 2005). Material was transported in a covered truck to a burial site remote from Darwin (A. Daly, personal communication). Continued surveillance led to two separate detections (and removal) in 2006. There were no further detections during the following 12 months, so Australia was declared free of the disease (Carroll, 2007).
The endemic diseases net blotch (Pyrenophora teres) and leaf scald (Rhynchosporium secalis) of winter barley were initially observed to be less severe where carry-over stubble of a previous crop was burnt or incorporated by cultivation than where it was only partially buried in experiments at Rothamsted in the UK (Jenkyn et al., 1995). However, by summer in the same crops both diseases were usually more severe where straw had been burnt than where it had been incorporated into soil.
Pruning and selective removal
For eradication of pathogens from perennial plants, an alternative to complete crop removal is pruning and selective removal of infected plants. This will reduce production loss and has potential to eradicate the pathogen in some cases. The successful eradication of canker, caused by the fungus Nectria galligena, from apple trees on the island of Tasmania in Australia, began in 1954 and spanned 20 years (Ransom, 1997). The programme combined complete removal of severely infected trees and pruning of infected wood from slightly infected trees. Bordeaux mixture fungicide was used to reduce risk of further infection and excised plant material was burned on site. Three surveys over the following 17 years failed to detect the disease. Twig canker, caused by Phomopsis arnoldiae, was eradicated from Bohemian olive in Arezzo, Italy by removal and elimination of infected plant parts and application of copper treatment after leaf fall (Marino, 2005). Anthracnose (Colletotrichum sp.) on tamarillo (Solanum betaceum) was controlled in Colombia by pruning of infected branches, removal of infected fruit and the use of fertilizers and protectant fungicides (Gomez Hurtado, 1993). However, the means by which infected material was destroyed was not reported.
Huanglongbing (HLB) disease of citrus trees, caused by the phytoplasma ‘Candidatus Liberibacter asiaticus’ and ‘Ca. Liberibacter americanus’, was first reported in Brazil in March 2004. Lopes et al. (2007) conducted experiments to determine if pruning of branches with symptoms or the entire canopy would eliminate the disease. Orange trees with different degrees of symptom severity as well as symptomless controls were pruned, although no detail on the method of disposal of infected plant material was provided. Caging and treatment with insecticides was used to control the psyllid vector, Diaphorina citri. Symptoms reappeared following pruning, with greater severity on trees with a greater degree of symptom severity before pruning. The failure of pruning to eradicate HLB may be due to the systemic nature of the pathogen, as only plant material showing symptoms was removed and the phytoplasma may have remained in symptomless tissue.
In a review of eradication measures in Ghana for over 40 years to control or contain the spread of Cocoa swollen shoot virus (CSSV), Thresh & Owusu (1986) concluded that removing only trees expressing symptoms was effective only in small outbreaks. It was more effective to selectively remove trees with symptoms as well as adjacent symptomless trees, although detail on the disposal of plant material was not offered.
Composting is the decomposition of biodegradable organic matter and generally consists of an initial mixing period with mesophilic (15–40°C) growth, a high temperature thermophilic (> 45°C) phase where ‘sanitization’ occurs, and another longer and lower temperature mesophilic phase for maturation or stabilization (Day & Shaw, 2001).
Composting has been the subject of research to eradicate fungal pathogens from contaminated plant debris. Fusarium oxysporum f.sp. melonis, the cause of vascular wilt of cucurbits, was eradicated after infected tissue was composted for at least 4 days at above 55°C (Suarez-Estrella et al., 2003). Club root (Plasmodiophora brassicae) was eradicated from infected brassica wastes after 7 days of composting at 54–73°C, assessed using a Chinese cabbage bioassay (Fayolle et al., 2006). The oomycete Phytophthora ramorum, causal agent of sudden oak death, could not be detected by PCR assay on inoculated leaves of California bay laurel following composting at 55°C (Swain et al., 2006). However, the fungus that causes dry root rot of beans and other crops in warm climates, Macrophomina phaseolina, survived a peak compost temperature of 60°C for 21 days (Lodha et al., 2002). A review by Noble & Roberts (2004) revealed that 33 of 38 fungal pathogens examined were reduced to levels below detection limits when exposed to peak composting temperatures of 64–70°C for 21 days.
Green waste such as tree, shrub, turfgrass and other landscape plant trimmings and weeds from home gardens and commercial landscapes is ground and used as mulch for ornamental landscapes and in avocado orchards in the USA. Downer et al. (2008) assessed survival of introduced plant pathogens in unturned piles of fresh and aged green waste which reached temperatures of 70°C and 45°C, respectively. Sclerotia of Sclerotinia sclerotiorum survived for 8 weeks in both fresh and aged green waste. In fresh green waste, Armillaria mellea and the nematode Tylenchulus semipenetrans did not survive more than 2 days and Phytophthora cinnamomi persisted for over 21 days. Composted aged green waste was less effective at reducing pathogen viability, most likely due to the cooler temperatures of 45°C rather than 70°C. It was concluded that sclerotium-forming pathogens are the most difficult to eradicate from undisturbed piles of green waste, and that intermittent turning of piles would increase the likelihood of eradication through increased temperature, microbial attack and chemical degradation.
Noble & Roberts (2004) listed four bacterial plant pathogens reported from the literature to be eradicated during composting. Composting conditions required for eradication were: 7 days at 40°C for E. amylovora on cotoneaster shoots; 77 days at 60°C for Erwinia chrysanthemi on chrysanthemum bark; 4 days at 35°C for Pseudomonas savastanoi on bean leaves; and 16 h at 59°C for Ralstonia solanacearum on potato. Noble & Roberts (2004) also reported the potential of composting for eradication of plant viruses quoting various examples. Tobacco mosaic virus (TMV) was eradicated from infected plant material after peak compost temperatures in excess of 68ºC and composting for longer than 28 days, although it is important to note that the conditions required for eradication vary in the literature. Other examples included the viral/fungal complexes Lettuce big vein virus (LBVV)/Olpidium sp. and Tobacco necrosis virus (TNV)/Olpidium sp. eliminated by composting at 50°C for 7 and 50 days, respectively, and Melon necrotic spot virus, TNV and Tomato spotted wilt virus eradicated by a peak composting temperature of 65°C and a composting duration of up to 28 days.
There is evidence that certain plant pathogens, with resting spores that may be heat tolerant, can survive composting, sometimes through inadequate methods or failures in the treatment process (Anon, 2008b). Examples reported from the literature include some formae speciales of Fusarium oxysporum, Olpidium brassicae, Plasmodiophora brassicae, Streptomyces scabies, TMV, Tobacco rattle virus (TRV) and Xanthomonas malvacearum (Noble & Roberts, 2004). In the European and Mediterranean Plant Protection Organization (EPPO) region, it has been recommended that plant material of origin known or suspected to contain any quarantine pathogens should receive additional heat treatment of 74°C for 4 h, 80°C for 2 h or 90°C for 1 h before or after composting (Anon, 2008b).
Methyl bromide has been used as a soil fumigant for almost 50 years and has a wide spectrum of activity against plant pathogens and pests, including fungi and bacteria. Its volatility allows good penetration of the soil through vapour diffusion and it has been used extensively to prepare soil for planting strawberry, tomato, pepper, tobacco, melons, grapes, ornamentals and turf grass for the successful control of pathogens such as Verticillium, Phytophthora, Pythium, Cylindrocarpon and Rhizoctonia spp. (Wilhelm & Paulus, 1980; Ristaino & Thomas, 1997; Porter et al., 1999; Duniway, 2002). Due to the environmental impact of methyl bromide on depletion of ozone, the use of this fumigant has been phased out as part of the Montreal Protocol, with an exception for use in the event of eradication (Duniway, 2002).
Alternatives to methyl bromide have been the subject of much research since the Montreal Protocol and several reviews (Ristaino & Thomas, 1997; Porter et al., 1999; Duniway, 2002; Ajwa et al., 2003; Ruzo, 2006) identify alternative chemical fumigants. Strawberry diseases caused by Rhizoctonia, Phytophthora and Verticillium spp. can be controlled using chloropicrin, 1,3-dichloropropene (Telone), or a mixture of both. Methyl iodide and sodium azide have efficacy against fungi similar to methyl bromide, but require application of greater rates. Dazomet (Basamid) also gave similar efficacy against soil fungi to methyl bromide. Methyl isothiocyanate, the primary active agent of metam sodium (Vapam), has activity against plant pathogenic fungi. However, distribution in soil is limited and if soil temperature and moisture are not optimal, methyl isothiocyanate may be unreliable. Application of chemical fumigant requires covering of the soil with plastic to contain the gas (Matthiessen & Kirkegaard, 2006).
Biofumigation refers to the suppression of selective soil-borne organisms by volatile isothiocyanates released by hydrolysis of glucosinolates from the decomposing tissues of Brassica spp. incorporated into the soil as a green manure (Matthiessen & Kirkegaard, 2006). An Australian study demonstrated that Indian mustard (B. juncea) green manure reduced the severity of bacterial wilt (R. solanacearum) in the following tobacco crop (Akiew & Trevorrow, 1999). Following greenhouse trials in Israel, Tsror et al. (2007) concluded that biofumigation can reduce the population of soil-borne pathogens such as F. oxysporum, R. solani, V. dahliae and Pythium spp. but not necessarily eradicate them. In vitro experiments by Fan et al. (2008) in China showed that powdered tissue of B. oleracea var. caulorapa on agar suppressed the growth of a wide range of soil-borne fungal species. Biofumigation reduced the number of viable microsclerotia of Verticillium spp. in field soil by 19–47% in Switzerland (Michel et al., 2007).
Limitations of biofumigation include containment of isothiocyanates within the soil, timing of incorporation so that soil moisture and temperature are optimal, and the increased occurrence of pathogens common to Brassica spp. (T. Wicks, personal communication). Biofumigation does not provide 100% mortality and therefore may not be suitable for eradication, but could be used as part of an integrated programme to assist in containing soil-borne disease without adverse impact on the environment.
Solarization, also known as polyethylene or plastic mulching, is the process in which clear polyethylene is placed over soil and utilises solar energy to raise the temperature for the control of soil-borne pests and diseases (Katan, 1981). Katan et al. (1976) suggested that biological as well as thermal activity may be involved in the suppression of soil-borne pathogens. Solarization is more economical and less hazardous than chemical fumigation.
There are numerous examples of the use of solarization in both the eradication and control of plant pathogens. Phytophthora nicotianae and R. solani were eradicated from tomato seed beds using double-layer solarization (Rodriguez Perez et al., 2005). Maximum temperatures at 5 cm depth in double layer-solarized seed beds were 70 and 73°C in 2002 and 2003, respectively, over 20ºC higher than the uncovered control. In both years, temperatures higher than 60°C over nine consecutive hours were achieved. Sclerotia of Corticium rolfsii were eradicated when solarization treatment was applied for 1 day at 60–80°C (Martins et al., 2003) and, in another study, were eliminated in potted soil at depths to 10 cm by solarization with polyethylene sheets for up to 21 days (Rao & Maity, 2003). Amendment of field soils with cabbage leaf residues in combination with soil solarization resulted in complete elimination of F. oxysporum f.sp. gladioli (gladiolus wilt) at 5 cm soil depth (Harender & Sachin, 2005). Verticillium dahliae was eliminated from soil to a depth of 25 cm after 2 weeks under polyethylene sheets in Israel (Katan et al., 1976). Fusarium oxysporum f.sp. lycopersici populations were reduced by 54–100% at varying depths to 25 cm and maximum soil temperatures in both cases were 49 and 42°C at 5 and 15 cm, respectively. Wilt of strawberry caused by F. oxysporum f.sp. fragariae was controlled under glasshouse conditions by soil solarization combined with solar-heated irrigation when heated at 40ºC for 7 days or at 45ºC for 2 days (Sugimura et al., 2001).
Effective solarization depends on soil type, moisture and pH and also requires warm, sunny days, limiting the timing and location of its use (T. Wicks, personal communication). A further limitation of soil solarization is the depth of penetration of temperatures necessary to kill the pathogen and it may therefore be more effective in combination with fumigation. In Spain, R. solanacearum and Tomato mosaic virus in tomato crops were successfully controlled by biosolarization (biofumigation with solarization), although temperature and time of exposure were not reported (Zanon et al., 2006).
Steam sterilization of soil surrounding infected trees (Cotoneaster and Sorbus) was used in the successful eradication of fire blight in Melbourne described previously. In Italy Sclerotium rolfsii, Fusarium oxysporum and Rhizoctonia solani were eradicated from field soil by steam sterilization during 1999–2006 using an Ecostar 600 self-propelled steriliser and a system of spray booms for steam (Perruzi, 2007). Whilst little information can be found on use of this method, it offers potential for use in eradicating soil-borne pathogens in the future.
Vectors such as insects may spread some plant pathogens, therefore controlling the vector is a viable method of containing a pathogen and could be used in an eradication programme in combination with cultural management techniques and destroying infected plant material. Although vectors occasionally spread bacterial and fungal pathogens, viral pathogens are commonly spread this way and there are many examples of vector control. The use of an insecticide for controlling mealybug vectors improved the likelihood of eradication of CSSV along with the adoption of virus-resistant cocoa cultivars (Thresh & Owusu, 1986). The use of aphid vector monitoring systems to assist the control of the spread of Potato virus Y, Barley yellow dwarf virus and Beet yellows virus is now well established as a tool to manage virus disease outbreaks (Sigvald, 1998; Anon, 2008a). Control is achieved through focused use of insecticides, crop-sowing timing, and the planting of resistant cultivars. A combination of resistant cultivars and cultural management of beet crops to provide early plant emergence and development, and a highly coordinated beet leafhopper vector scouting and spray programme have achieved adequate control of Beet curly top virus in California, USA (Wisler & Duffus, 2000). Similarly, soil-borne viruses such LBVV, TNV and TRV can be managed using host resistance combined with chemical treatment of the soil-borne vector (Walsh, 1998).
Biological control is the use of beneficial organisms and their products, such as metabolites, which reduce the negative effects of plant pathogens and promote positive responses by the host plant (Vinale et al., 2008). Trichoderma spp. and Bacillus spp. are among the most commonly isolated soil microorganisms which produce biologically active compounds, such as cell wall degrading enzymes and secondary metabolites. Their ability to protect plants and contain pathogen populations has led to these fungi being widely studied (Cannon, 1996; Vinale et al., 2008). Biological control of Pierce's disease (Xylella fastidiosa) through inoculation with benign strains of the bacterium was reported to have potential for commercial vineyards according to Hopkins (2005).
Bacteriophages are viruses that multiply inside bacterial cells and may offer a method of biological control of bacterial pathogens. In the field, reduced bacterial populations of X. campestris pv. juglandis were associated with substantial increases in phage numbers, suggesting involvement of the latter in controlling walnut blight (McNeil et al., 2001). Citrus canker and bacterial spot caused by X. axonopodis pvs. citri and citrumelo were controlled in the greenhouse by bacteriophage treatment (Balogh et al., 2008). However, the efficacy of phages, as is true of many biological control agents, depends greatly on prevailing environmental factors as well as on susceptibility of the target organism (Jones et al., 2007).
Biological control is not normally appropriate for eradication of a pathogen. However, if used for this purpose it would require inundative application of the biocontrol agent in numbers sufficient to overwhelm the pathogen population and possibly combined with other treatments in an integrated programme (Ebbels, 2003).
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- Eradication case studies
- Techniques for eradication and containment of plant pathogens
Eradication or containment of exotic plant pathogens requires great effort from all those involved. Along with many successful eradication schemes there have been failures. Usually due to the integrated approach required in undertaking eradication it is often difficult to identify specific reasons for success or failure. In this review, examples from the literature have been described, methodologies summarized and available evidence examined for some of the successes.
Burning infected plant material has been widely used in the eradication and control of exotic and endemic pathogens. However, there appears to be little or no scientific evidence available to confirm that pathogens are eliminated during this process. Murray (1998) suggested that destroying wheat crops with Karnal bunt by burning could be counterproductive, as spores of the pathogen may rise in the heat currents and be dispersed, effectively spreading disease which, along with survival of spores in soil, was reported from unpublished data (Sansford et al., 2004). Several studies have shown temperature is a crucial factor in pathogen mortality, so burn-temperatures need to be above a certain threshold over a period of time. In his review, Hardison (1976) concluded that the effectiveness of burning for disease control needs to be determined for individual diseases, and that a limitation of this strategy is the incomplete burning of residues. Further research is necessary to increase confidence in burning for elimination of pathogens.
Burial of infected plant material, with or without burning, is also commonly used in eradication programmes. The likelihood of pathogen dispersal and survival or decline on either buried or exposed material needs to be considered. There is a great deal of published information on epidemiological factors affecting survival of specific plant pathogens. The most important decision when burying is where to bury, the depth at which material should be placed, and should include consideration of drainage or seepage (T. Wicks, personal communication). The buried material should be covered with a depth of soil which prevents disturbance by birds, animals or the elements; Ebbels (2003) suggests at least 2 m. Burial at 2 m was used in the fire blight eradication in Melbourne (Rodoni et al., 1999), but burial depth was not specified in literature concerning any other examples. Further research on pathogen survival on different plant material, soil types and under different environmental conditions could provide evidence for the optimal burial conditions for a successful eradication. Burial is an effective method of disposal but, where possible, should be done on-site. Processing of the material, such as chipping, may increase the decomposition of wood, but also increases chances of pathogen dispersal. On-site disposal of plant material is sometimes not practical in urban situations. For example, during the eradication of grapevine leaf rust in Darwin, plant material was removed, isolated and transported carefully to a remote site to avoid dispersal of infected material (A. Daly, personal communication).
Complete removal of perennial crops for eradication of pathogens can lead to substantial economic loss to industries. The use of severe pruning to remove infected parts of the plant and reworking from the trunk minimises the time taken to restore it to commercial productivity. This method was used as part of the successful eradication of black Sigatoka on bananas in Tully and nectria canker from apples in Tasmania, and was reported to contribute to the control of citrus canker and huanglongbing in Brazil, as well as anthracnose of tamarillos in Columbia. Eradication of non-systemic exotic pathogens such as these in other hosts requires research to develop specific protocols.
Biological control has been commonly employed to control endemic plant pathogens, but due to its variable nature has not been considered for eradication of exotic pathogens. However, there may be potential for its use as part of an integrated approach, especially for containing an outbreak. Bacteriophage may provide a promising strategy in the control of fire blight. Bacteriophages isolated from E. amylovora have shown a high degree of lytic activity against E. amylovora in the laboratory, but there have been no studies to determine the effectiveness of the phage as a control agent in the orchard environment. To date, E. amylovora lytic phage has been investigated only in areas where fire blight is endemic in the USA (Schnabel et al., 1999) and Canada (Svircev et al., 2002). Australian orchards have remained free of fire blight and this may be due in part to the presence of some natural defence mechanisms in those orchards in the form of a natural antagonist of E. amylovora such as an aggressive bacteriophage. There is evidence for a unique microflora consisting of closely related saprophytic Erwinia species in Australian orchards, which requires further investigation (Rodoni et al., 2003).
Plant viruses and virus diseases have been studied for more than 100 years and much attention has been given to their control (Thresh, 2003). Chemotherapy, thermotherapy and meristem-tip culture can be successful, but they cannot be routinely used on a large scale. Consequently, the main approach has been to prevent or delay a virus infection or to ameliorate its effects. Various means have been used to achieve these objectives, including phytosanitation (involving quarantine measures, crop hygiene, use of virus-tested planting material and eradication), timing of crop planting, use of pesticides to control vectors, mild strain protection and the deployment of resistant or tolerant cultivars. These measures can be used singly or in combination to exploit synergistic interactions. The strategy of removing infected plants for eradication of virus diseases has often been attempted with perennial crops such as fruit trees or grapes. According to Thresh (1988), the success of this strategy for eradication or containment depends on the rapidity of implementation following an incursion and the extent of knowledge on the epidemiology of the disease and the availability of detection methods.
Composting plant material may also provide an alternative to burning and/or burying during the eradication of exotic pathogens, however, additional heat treatment is recommended in the EPPO-region to ensure sterilization of plant material containing quarantine pathogens (Anon, 2008b). The success of composting is largely dependent on the exposure of pathogens to certain temperatures and time periods sufficient to kill the pathogen. If successful this strategy has the potential to be integrated into a containment and/or eradication programme.
Soil-borne pathogens are particularly difficult to eradicate. The use of one, or a combination of, solarization, chemical fumigation or biofumigation may provide support in controlling a pathogen incursion but efficacy and consistency remain uncertain.
In conclusion, there are many examples to draw upon in considering methods of eradication and a sound understanding of the biology and epidemiology of a pathogen is paramount. The information available from past eradications is not always sufficiently detailed and so more effort is required to produce and publish scientific evidence to support the success or otherwise of attempts of containment and eradication of incursive plant pathogens and diseased plant material.
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- Eradication case studies
- Techniques for eradication and containment of plant pathogens
This review was supported by the Cooperative Research Centre for National Plant Biosecurity and New Zealand – Better Border Biosecurity B3 programme. The authors thank Trevor Wicks (South Australian Research and Development Institute) and Eileen Scott (University of Adelaide) for reviewing the manuscript and George Gill and Karen Froud (Ministry of Agriculture & Forestry, Biosecurity, New Zealand) for helpful discussions and comment.
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- Eradication case studies
- Techniques for eradication and containment of plant pathogens
- 2002. Powdery mildew – a new disease of horse chestnut in Poland. Ochrona Roslin 46, 12–3. , , ,
- 2003. Alternatives to methyl bromide in strawberry production in the United States of America and the Mediterranean region. Phytopathologia Mediterranea 42, 220–44. , , et al .,
- 1999. Biofumigation of bacterial wilt of tobacco. In: Proceedings of the First Australasian Soil-Borne Disease Symposium, 1999. Brisbane, Australia: Australasian Plant Pathology Society, 207–8. , ,
- Anonymous, 2003. Commission Directive 2003/116/EC. Official Journal of the European Union L321/36 6.12.2003 [http://eur-lex.europa.eu.
- Anonymous, 2007. Glossary of Phytosanitary Terms. International Standards for Phytosanitary Measures No. 5. Food and Agriculture Organization of the United Nations – International Plant Protection Convention. [http://www.ippc.int/IPP/En/default.jsp]
- Anonymous, 2008a. Aphidwatch – Cereal, Potato, Squash and Lettuce. [http://www.aphidwatch.com/]
- Anonymous, 2008b. Guidelines for the management of plant health risks of biowaste of plant origin. PM 3/66 (2), EPPO Bulletin 38, 4–9.
- 2008. Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Disease 92, 1048–52. , , , ,
- 1999. A geophytopathological study of fire blight in a pear growing area of the Po Valley (Northern Italy). Acta Horticulturae 489, 93–7. , , ,
- 2005. Citrus canker sanitation in groves by drastic pruning. In: Proceedings of the Second International Citrus Canker and Huanglongbing Research Workshop, 2005. Orlando, FL, USA, 24. , , ,
- 1974. Fireblight in Hawthorn in England and Denmark. Plant Pathology 23, 141–3. , , ,
- 1993. Effects of rotation, stubble retention and cultivation on take-all and eyespot of wheat in North Eastern Victoria, Australia. Soil & Tillage Research 25, 263–80. de, , , ,
- 1995. A further outbreak of citrus canker near Darwin. Australasian Plant Pathology 24, 90–103. , , et al .,
- 1996. Plant Viruses Online: Descriptions and Lists from the VIDE Database. Version: 20th August 1996. [http://biology.anu.edu.au/Groups/MES/vide/] , , , , , ,
- 1996. Control of Fusarium crown rot of wheat by late stubble burning and rotation with sorghum. Australasian Plant Pathology 25, 229–33. , , , ,
- 1999. A severe unforeseen outbreak of fire blight in the Emilia-Romagna region. Acta Horticulturae 489, 171–6. , , ,
- 1996. Bacillus thuringiensis use in agriculture: a molecular perspective. Biological Reviews 71, 561–636. ,
- 2007. Grapevine Leaf Rust – Current Status. Northern Territory Department of Primary Industry, Fisheries and Mines. [ http://www.nt.gov.au/d/Primary_Industry/vinerust/index.cfm?header=Current%20Status ] ,
- 1940. Black spot or scab of apples. Serious new outbreaks recorded in the Albany and Manjimup districts. Western Australian Journal of Agriculture 17, 56–67. ,
- 1948. Apple scab outbreaks season 1947–48, with special reference to the introduction of the disease by infected buds on imported nursery stock. Western Australian Journal of Agriculture 25, 129–35. , , ,
- 1993. Eradication of apple scab. Western Australian Journal of Agriculture 34, 146–9. , ,
- 2001. Biological, chemical and physical processes of composting. In: StoffellaPJ, KahnBA, eds. Compost Utilization in Horticultural Cropping Systems. Boca Raton, FL, USA: Lewis Publishers, 17–50. , ,
- 1997. Eradication of Apple Scab in Western Australia 1989–97. South Perth, Western Australia: Agriculture Western Australia. ,
- 2008. Survival of plant pathogens in static piles of ground green waste. Phytopathology 98, 547–54. , , et al .,
- 2002. Status of chemical alternatives to methyl bromide for pre-plant fumigation of soil. Phytopathology 92, 1337–43. ,
- 1960. Citrus canker is still in New Zealand. The Orchardist of New Zealand August, 199–201. ,
- 2003. Principles of Plant Health and Quarantine. Wallingford, UK: CABI Publishing. ,
- 2008. Potential biofumigation effects of Brassica oleracea var. caulorapa on growth of fungi. Journal of Phytopathology 156, 321–5. , , , , ,
- 2006. Eradication of Plasmodiophora brassicae during composting of wastes. Plant Pathology 55, 553–8. , , , , ,
- 2006. Managing outbreaks of invasive species: eradication versus suppression. International Journal of Pest Management 52, 261–8. , , , , ,
- 2006. New to New Zealand: detection of common smut of corn (Ustilago maydis) from a single cornfield in Gisborne. New Zealand Plant Protection 59, 373. , , , , , ,
- 2007. Evaluation of potential citrus canker inoculum reservoirs in Emerald, Queensland. In: Proceedings of the Sixteenth Australasian Plant Pathology Conference, 2007. Adelaide, Australia: Australasian Plant Pathology Society, 68. , , , , ,
- 2006. Management options for minimizing the damage by ascochyta blight (Ascochyta rabiei) in chickpea (Cicer arietinum L.). Field Crops Research 97, 121–34. , , , ,
- 2008. Soil solarisation to eradicate boil smut. Biosecurity 82, 14. ,
- 1993. Evaluation of fungicides and some agricultural practices for the control of anthracnose on tamarillos in Sotara (Cauca). ASCOLFI Informa 19, 24–5. ,
- 2001. The citrus canker epidemic in Florida: the scientific basis of regulatory eradication policy for an invasive species. Phytopathology 91, 30–4. , , , , ,
- 2007. Post-hurricane analysis of citrus canker II: predictive estimation of disease spread and area potentially impacted by various eradication protocols following catastrophic weather events. Plant Health Progress April, 1–15. , ,
- 2004. Xanthomonas axonopodis pv. citri: factors affecting successful eradication of citrus canker. Molecular Plant Pathology 5, 1–15. , , , ,
- 1976. Fire and flame for plant disease control. Annual Review of Phytopathology 14, 355–79. ,
- 1980. Role of fire for disease control in grass seed production. Plant Disease 64, 641–5. ,
- 2005. Integration of soil solarization with cruciferous leaf residues for the control of Fusarium wilt pathogen of gladiolus. Integrated plant disease management. In: Challenging Problems in Horticultural and Forest Pathology, Solan, India, 14 to 15 November 2003. Jodhpur, India: Scientific Publishers, 215–20. , ,
- 1965. Erwinia amylovora. CMI Descriptions of Pathogenic Fungi and Bacteria, No. 44. Wallingford, UK: CAB International. , ,
- 1918. History of Citrus Canker in the Northern Territory. Bulletin of the Northern Territory of Australia, No. 18. ,
- 2005. Biological control of Pierce's disease in the vineyard with strains of Xylella fastidiosa benign to grapevine. Plant Disease 89, 1348–52. ,
- 2002. The use of hierarchical sampling in the National Surveillance Program for Plum pox virus incidence. Plant Disease 86, 259–63. , , ,
- 1995. Effects of incorporating straw, using different cultivation systems, and of burning it, on diseases of winter barley. Journal of Agricultural Science 124, 195–204. , , ,
- 2000. Screening of ornamental plants from the Botanic Gardens of Melbourne and Adelaide for the occurrence of Erwinia amylovora. Australasian Plant Pathology 29, 120–8. , , et al .,
- 1984. Failure of the black Sigatoka eradication program in the Torres Strait region. Australasian Plant Pathology 13, 57–8. ,
- 1991. Successful eradication of citrus canker from Thursday Island. Australasian Plant Pathology 20, 89–91. ,
- 1984. Citrus canker on Thursday Island, Australia. Australasian Plant Pathology 13, 64–5. , , ,
- 2007. Bacteriophages for plant disease control. Annual Review of Phytopathology 45, 245–62. , , , , , ,
- 1981. Solar heating (solarization) of soil for control of soil-borne pests. Annual Review of Phytopathology 19, 211–36. ,
- 1976. Solar heating by polyethylene mulching for the control of diseases caused by soil-borne pathogens. Phytopathology 66, 683–8. , , , ,
- 2005. Prevalence and survival, with emphasis on stubble burning, of Rhizoctonia spp., causal agents of sheath diseases of rice in Australia. Australasian Plant Pathology 34, 135–42. , , , , , ,
- 2006. Plum pox virus in the United States of America. EPPO Bulletin 36, 217–8. ,
- 2000. First report of plum pox virus (Sharka disease) in Prunus persica in the United States. Plant Disease 84, 202. , , ,
- 1998. Strawberries. Bacterial disease Xanthomonas in strawberries. Proeftuinnieuws 8, 49–50. ,
- 2004. Investigation of the occurrence of banana wilting disease and its control. South China Fruits 33, 64–5. ,
- 2002. Inactivation of Macrophomina phaseolina propagules during composting and effect of composts on dry root rot severity and on seed yield of cluster bean. European Journal of Plant Pathology 108, 253–61. , , ,
- 2007. Ineffectiveness of pruning to control citrus huanglongbing caused by Candidatus Liberibacter americanus. European Journal of Plant Pathology 119, 463–8. , , , , ,
- 1996. Apple Scab – Biology, Epidemiology and Management. St Paul, MN, USA: APS Press. ,
- 2005. Phomopsis arnoldiae. Stem canker on Bohemian olive. Sherwood – Foreste ed Alberi Oggi 116, 47–8. ,
- 2003. Eradication of Sclerotium rolfsii sclerotia in substrate treated in solar collector devices in Campos dos Goytacazes-RJ. Revista Brasileira de Fruticultura 25, 421–4. , , , ,
- 2006. Biofumigation and enhanced biodegradation: opportunity and challenge in soil-borne pest and disease management. Critical Reviews in Plant Sciences 25, 235–65. , ,
- 2001. Apple scab successfully eradicated in Western Australia. Australasian Plant Pathology 30, 371. , , ,
- 2001. Bacteriophages: a potential biocontrol agent against walnut blight (Xanthomonas campestris pv. juglandis). New Zealand Plant Protection 54, 220–4. , , , , , ,
- 1952. Plant quarantine survey in the Northern Territory. Journal of the Australian Institute of Agricultural Science 18, 27–32. ,
- 2007. Biofumigation, a control method for soil-borne diseases. Revue Suisse de Viticulture, Arboriculture et Horticulture 39, 145–50. , , ,
- 1974. Mycosphaerella fijensis. CMI Descriptions of Pathogenic Fungi and Bacteria, No. 413. Wallingford, UK: CAB International. , ,
- 1998. Pest Risk Analysis on Karnal Bunt of Wheat. Risk Analysis Report. Wagga Wagga, Australia: NSW Agriculture. ,
- 1998. The risk to Australia from Tilletia indica, the cause of Karnal bunt of wheat. Australasian Plant Pathology 27, 212–25. , ,
- 2006. Control and monitoring: monitoring and eradication of sharka in south-east Italy over 15 years. EPPO Bulletin 36, 309–11. , , , ,
- 2004. Eradication of plant pathogens and nematodes during composting: a review. Plant Pathology 53, 548–68. , ,
- 1994. Diseases caused by bacteria on Cucurbitaceae. Informe Agropecuario (Belo Horizonte) 17, 54–7. , ,
- 1989. Bacterial plant diseases. In: PennycookS, ed. Plant Diseases Recorded in New Zealand, Vol. 3. Auckland, New Zealand: Auckland Plant Diseases Division DSIR, 23–83. , , ,
- 1996. Witches’ broom disease of cocoa in Bahia: attempts at eradication and containment. Crop Protection 15, 743–52. , , ,
- 2007. L’Attivita Attivita’ di Ricerca Svolta sul Sistema Bioflash Nel Periodo 1999–2006. Pisa, Italy: Università di Pisa. [ http://www.avanzi.unipi.it/ricerca/convegni/giornata_dimo_vapore/documenti_giornata_vapore/peruzzi_ciraa_cell_2007.pdf ] ,
- 2002. Black Sigatoka Eradication – Controlled Management Program, Tully Banana Production Area. Queensland, Australia: Queensland Department of Primary Industries. ,
- 2005. Eradication of black leaf streak disease from banana growing areas in Australia. InfoMusa 14, 7–10. , , ,
- 2000. Ascospore survival in banana leaf trash. Bananatopics 28, 5–6. , , ,
- 1995. Eradication of citrus canker from Australia. Pacific Association of Tropical Phytopathology News 13, 1–2. , ,
- 1936. Black spot or scab of apples. Western Australian Journal of Agriculture 21, 241–63. ,
- 1999. Alternatives to methyl bromide: chemical fumigants or integrated pest management systems? Australasian Plant Pathology 28, 65–71. , , ,
- 1944. The eradication of black spot or apple scab in Western Australia. Western Australian Journal of Agriculture 21, 148–55. , ,
- 1997. The eradication of Nectria galligena from apple trees in Tasmania, 1954 to 1991. Australasian Plant Pathology 26, 121–5. ,
- 2003. Solar heating by polyethylene mulching for the control of collar rot of chilli caused by Sclerotium rolfsii Sacc. Journal of Mycopathological Research 41, 193–6. , ,
- 1938. Citrus canker in New Zealand. New Zealand Journal of Science & Technology 20A, 55–62. ,
- 1999. Control of fire blight in pears by in situ flamation of blighted shoots and blossoms. Acta Horticulturae 489, 573–6. , , ,
- 1997. Agriculture, methyl bromide, and the ozone hole: can we fill the gaps? Plant Disease 81, 964–77. , ,
- 1999. Detection of Erwinia amylovora, the causal agent of fire blight, in the Royal Botanic Gardens, Melbourne, Australia. Acta Horticulturae 489, 169–70. , , , , ,
- 2002. National surveys did not detect Erwinia amylovora on host plants in Australia. Acta Horticulturae 590, 39–45. , , , , , ,
- 2006. Costs associated with fire blight incursion management and predicted costs of future incursions. Acta Horticulturae 704, 55–61. , , , ,
- 2003. Taxonomic Relationships and Biology of Erwinia amylovora and Related Bacteria Isolated from Ornamental Plants in South Eastern Australia. Report to Horticulture Australia Limited, Project No. IHD024. , , ,
- 2005. Eradication of Phytophthora nicotianae and Rhizoctonia solani by double layer solarization in tomato seedbeds. Acta Horticulturae 698, 207–11. , , ,
- 2006. Physical, chemical and environmental properties of selected chemical alternatives for the pre-plant use of methyl bromide as soil fumigant. Pest Management Science 62, 99–113. ,
- 2004. Evaluation of Published Data on the Efficacy of ‘Other’ (Non-Fungicide) Control Strategies for Tilletia indica (Karnal Bunt) including the Control of Soil-Borne Inoculum and the Treatment of Infected Grain or Seed. EC Fifth Framework Project QLK5-1999-01554 Deliverable Report: DL 6.3. [ http://karnalpublic.pestrisk.net/deliverables] , , ,
- 2008. The new Pest Risk Analysis for Tilletia indica, the cause of Karnal bunt of wheat, continues to support the quarantine status of the pathogen in Europe. Plant Pathology 57, 603–11. , , et al. ,
- 2005. Reclassification of Xanthomonas campestris pv. citri. Systematic and Applied Microbiology 28, 494–518. , , et al. ,
- 1999. Bacteriophage of Erwinia amylovora and their potential for biocontrol. Acta Horticulturae 489, 649–53. , , , , ,
- 1987. Citrus canker in Florida. Plant Disease 71, 388–95. , , et al. ,
- 2001. Meeting the challenge of eradicating citrus canker in Florida – again. Plant Disease 85, 340–56. , , , , , ,
- 1999. Development and evaluation of a decision support system for management of fire blight in pears. Acta Horticulturae 489, 385–92. , , , , , ,
- 2002. Coping with fire blight in pears: experience gained in Israel in the fire blight management (Fire-Man) project. Acta Horticulturae 590, 253–62. , , et al. ,
- 1998. Plant Virus Disease Control: Forecasting Aphid Transmitted Diseases. St Paul, MN, USA: APS Press. ,
- 2003. Eradication – preventing invasions at the outset. Weed Science 51, 247–53. ,
- 1993. Integrated management of wheat Karnal bunt. International Journal of Pest Management 39, 431–4. , , ,
- 1990. Fire blight in Norway. Acta Horticulturae 273, 37–40. ,
- 1993. Eradication of fire blight in Norway. Acta Horticulturae 338, 85–7. ,
- 2004. Experiences with the control of fire blight in Norway during 1986/2003. EPPO Bulletin 34, 361–3. , ,
- 1999. Report on the development and use of Cougarblight 98C – a situation specific fire blight risk assessment model for apple and pear. Acta Horticulturae 489, 429–36. ,
- 1990. Predicting apple blossom infections by Erwinia amylovora using the Maryblyt model. Acta Horticulturae 273, 139–48. ,
- 1980. Sigatoka leaf spots of banana and plantains. Plant Disease 64, 750–6. ,
- 2003. Temperature effect on Fusarium oxysporum f.sp. melonis survival during horticultural waste composting. Journal of Applied Microbiology 94, 475–82. , , , , ,
- 2001. Control of Fusarium wilt of strawberry by soil solarization using mulching and tunnel-covering combining with irrigation of solar-heated water. Bulletin of the Nara Prefectural Agricultural Experiment Station 32, 1–7. , , ,
- 2002. Biocontrol of Erwinia with bacteriophages. Bulletin OILB/SROP 25, 139–42. , , , , ,
- 2006. Composting is an effective treatment option for sanitization of Phytophthora ramorum-infected plant material. Journal of Applied Microbiology 101, 815–27. , , et al. ,
- 2002. Molecular detection of exotic phytopathogenic bacteria: a case study involving canker-like symptoms on citrus. New Zealand Plant Protection 55, 53–7. , , , ,
- 2007. National Citrus Canker Eradication Program Summary. Queensland Department of Primary industries and Fisheries. [ http://www.dpi.qld.gov.au/cps/rde/xchg/dpi/hs.xsl/4790_5370_ENA_HTML.htm ] ,
- 2006. Control and monitoring: control strategies for Plum pox virus in Canada. EPPO Bulletin 36, 302–4. ,
- 1988. Eradication as a virus disease control measure. In: CliffordBC, LesterE, eds. Control of Plant Diseases: Costs and Benefits. Oxford, UK: Blackwell Scientific Publications, 155–94. ,
- 2003. Control of plant virus diseases in sub-Saharan Africa: the possibility and feasibility of an integrated approach. African Crop Science Journal 11, 199–223. ,
- 1986. The control of cocoa swollen shoot disease in Ghana: an evaluation of eradication procedures. Crop Protection 5, 41–52. , ,
- 2007. Biofumigation for the control of soil-borne diseases. Acta Horticulturae 747, 389–94. , , et al. ,
- 1998. Outbreak and eradication of plum pox potyvirus in the Netherlands. Acta Horticulturae 472, 407–11. , , ,
- 2008. Occurrence and control of Plum pox virus in the Netherlands. Acta Horticulturae 781, 197–202. , , ,
- 2008. Trichoderma-plant-pathogen interactions. Soil Biology & Biochemistry 40, 1–10. , , , , , ,
- 2007. Identification of Banana Varieties with Resistance to Fusarium Wilt Tropical Race 4. Report to Horticulture Australia Limited, Project No. FR00043. , ,
- 1998. Plant Virus Disease Control: Chemical Control of Fungal Vectors of Plant Viruses. St Paul, MN, USA: APS Press. ,
- 2003. First record of grapevine leaf rust in the Northern Territory, Australia. Australasian Plant Pathology 32, 117–8. , , , ,
- 2005. Australia's grapevine leaf rust eradication program – the story so far. Australian Viticulture 9, 36–8. ,
- 1980. How soil fumigation benefits the California strawberry industry. Plant Disease 64, 264–70. , ,
- 2000. A century of plant virus management in the Salinas valley of California, ‘East of Eden’. Virus Research 71, 161–9. , ,
- 2005. A long-term strategy of sharka eradication in Poland. Phytopathologia Polonica 36, 137–41. , ,
- 2006. Biofumigation as a technique for the control of pathogenic viruses and bacteria. Bulletin OILB/SROP 29, 307–12. , , , ,