1IACR-Rothamsted, Harpenden, Herts. AL5 2JQ, UK
2ADAS Boxworth, Cambridge CB3 8NN, UK
3SAC, Bucksburn, Aberdeen AB21 9YA, UK
4Central Science Laboratory, MAFF, Sand Hutton, York YO41 1LZ, UK
Survey results show that the most serious diseases on winter oilseed rape in the UK are light leaf spot (Pyrenopeziza brassicae) and stem canker (Leptosphaeria maculans), then stem rot (Sclerotinia sclerotiorum) and dark pod spot (Alternaria brassicae); severity of epidemics differs between seasons, between regions and between crops. Diseases cause losses of up to £80M each season, despite expenditure of up to £12M on fungicides to control them. Light leaf spot is a polycyclic disease initiated in autumn (GS 1,05), probably by wind-borne ascospores, and spread by splash-dispersed conidia. Stem canker is a monocyclic disease; in autumn wind-borne ascospores infect leaves to cause phoma leaf spots and the pathogen grows down petioles to stems, on which canker lesions are observed in spring (GS 6,4). Regional forecasts predict risk of severe light leaf spot epidemics and can be modified by specific factors (e.g. cultivar, sowing date) to estimate risks in individual crops. A protocol for confirming the presence of light leaf spot involves sampling crops, incubating plants and assessing the appearance of diagnostic white pustules of the pathogen. Field experiments have suggested that growers need to consider control of light leaf spot and stem canker in autumn and late winter and control of stem rot and dark pod spot in spring.
KEYWORDS: Disease surveys, fungicide timing, light leaf spot, sampling, stem canker, yield loss.
Integrated management of diseases on winter oilseed rape, the most important arable crop in the UK after cereals (with >400,000 ha grown each season), depends on understanding their epidemiology and forecasting the risk of severe epidemics. Retrospective estimates of losses can be used to determine the importance of different diseases. Forecasting schemes, based on empirical relationships between measured disease incidence and earlier disease incidence or weather factors (e.g. temperature, rainfall), may be improved by incorporating information on the epidemiology of diseases (e.g. infection conditions, ascospore release). Furthermore, the presence of disease may be confirmed by sampling crops but methods are required for accurate diagnosis of pathogens at the time when spray decisions need to be taken. For both economic and environmental reasons, fungicide timing needs to be optimised so that only crops which require treatment are treated. This review describes work on estimating losses from winter oilseed rape diseases, on the epidemiology, diagnosis and forecasting of light leaf spot and stem canker, and on optimising fungicide use.
ESTIMATING LOSSES FROM DISEASES
Retrospectively, losses from diseases have been estimated by combining data from the ADAS/CSL winter oilseed rape disease survey for England and Wales and yield loss formulae for individual diseases. The survey, based on a stratified sample of commercial crops, provides information on the incidence and severity of diseases (e.g. Turner et al., 1999). Yield loss formulae have been derived for each disease from results of field experiments in which fungicide treatments have been used to manipulate incidence of diseases (e.g. Sansford et al., 1996). These estimates suggest that diseases can cause up to £80M of losses per season in winter oilseed rape (Fitt et al., 1997) but that losses differ greatly from season to season (Fig. 1). However, stem canker (Leptosphaeria maculans) and light leaf spot (Pyrenopeziza brassicae) are the two diseases which consistently cause the greatest losses. There are regional differences, with light leaf spot being most severe in the north of England and in Scotland (Sutherland et al., 1995) and stem canker being most severe in the east and south of England (Table 1). Furthermore, there are also differences between individual crops; severely affected crops may still occur in regions where the incidence of the disease is generally small. After stem canker and light leaf spot, the most serious problems are stem rot (Sclerotinia sclerotiorum) and dark pod spot (Alternaria brassicae), which can both cause serious losses in individual crops from time to time. Fungicide timing has not been optimal, despite expenditure of up to £12M on fungicides each season; crops requiring treatment have been left unsprayed at the appropriate time and others sprayed unnecessarily (Hardwick & Turner, 1994).
Fig. 1. Winter oilseed rape disease losses in England and Wales, estimated from ADAS/CSL survey data for seasons from 1986/87 to 1997/98 and yield loss formulae for each disease
An equation for prediction of yield loss from light leaf spot incidence on leaves at growth stage (GS) 3,3 (flower buds visible; Sylvester-Bradley & Makepeace, 1985) has been developed (Su et al., 1998). This relationship was based on results from experiments in Scotland, where light leaf spot was the only important disease, but fitted reasonably well to data from experiments in England with the same cultivar. The work now needs to be extended to produce a suite of models with different parameter values for different cultivars and different regions of the UK, which can be incorporated into a forecasting scheme. Furthermore, predictive models need to be derived for situations where a combination of diseases occurs together (e.g. much of England where both light leaf spot and stem canker occur). Models which provide information about risks of yield loss from stem canker or light leaf spot need to be available in the autumn (GS 1,05), which is the optimum time for controlling these diseases (Rawlinson et al., 1984; Figueroa et al., 1994), rather than at GS 3,3 in the spring, which is the last opportunity for applying a fungicide effectively.
EPIDEMIOLOGY OF LIGHT LEAF SPOT AND STEM CANKER
Not only are light leaf spot and stem canker the two most important diseases of winter oilseed rape in the UK, but also they differ greatly in their epidemiology (Table 1). Light leaf spot is a polycyclic disease, which infects leaves, stems, flowers and pods, with several pathogen life cycles occurring between sowing in August/September and harvest the following July (McCartney & Lacey, 1990). By contrast, stem canker is a monocyclic disease, with one life cycle per season, although there is an extended period from October to March over which stem lesions may be initiated by infection of different leaves (Gladders & Musa, 1980; Hammond & Lewis, 1986). Light leaf spot is caused by one pathogen, Pyrenopeziza brassicae, although there is evidence of genetic variability within the UK population (Majer et al., 1998). However, there are two distinct groups of Leptosphaeria maculans isolates in the UK (A group and B group), which are probably different species (Williams & Fitt, 1999) and cause different types of lesions on stems and leaves (Ansan-Melayah et al., 1997).
Table 1. Contrasting epidemiology of light leaf spot (Pyrenopeziza brassicae) and stem canker (Leptosphaeria maculans) on winter oilseed rape in the UK
Light leaf spot
Systemic (leaf →stem)
Long latent period
Long incubation period
Regional importance (UK)
North, West & Midlands
East, South & Midlands
The primary inoculum for stem canker epidemics is air-borne L. maculans ascospores, produced in pseudothecia on stem debris from previous crops (Gladders & Musa, 1980), which infect leaves to cause phoma lesions in autumn (GS 1,05). However, the role of air-borne ascospores of P. brassicae, produced in apothecia on stem and pod debris, in initiating epidemics of light leaf spot is less clear (McCartney & Lacey, 1990) and splash-dispersed conidia produced in acervuli on volunteer oilseed rape seedlings and vegetable brassica crops may also be involved. The optimum temperature for infection of oilseed rape leaves by L. maculans ascospores is c. 20°C; at this temperature the maximum number of lesions is greater than at lower (Fig. 2a) or higher temperatures (Biddulph et al., 1998). The optimum wetness duration at 20°C is c. 48 h; at shorter wetness durations (Fig. 2b) fewer lesions are formed and at longer wetness durations no more lesions are formed. By contrast, the optimum temperature for infection by P. brassicae conidia is c. 15°C (Figueroa et al., 1995). From infected leaves, L. maculans grows systemically down leaf petioles (on which no symptoms are visible) to reach the stems, on which lesions appear the following spring (GS 6,4; Hammond et al., 1985; Hammond & Lewis, 1986). However, there is little evidence that P. brassicae infects oilseed rape systemically; the disease spreads up plants through secondary spore dispersal and through extension of stems with infected meristematic tissue (Paul & Rawlinson, 1992).
P. brassicae has a biotrophic phase after infection followed by a necrotrophic phase (Ashby, 1997), whereas L. maculans has a necrotrophic phase on leaves followed by a systemic biotrophic phase in petioles. P. brassicae generally produces secondary spores (conidia) on living leaves, stems, flowers or pods before tissues die and symptoms appear (Paul & Rawlinson, 1992). However, L. maculans generally kills tissues and produces lesions on leaves or stems before conidia are produced in pycnidia in the dead tissue. Thus the latent period (between infection and sporulation) of P. brassicae (c. 200 degree-days; Figueroa et al., 1995) is shorter than the incubation period (between infection and symptom appearance), whereas the incubation period of L. maculans (c. 150 degree-days for leaf lesions; Biddulph et al., 1998; >200 days for stem lesions; Hammond & Lewis, 1986) is shorter than the latent period. Furthermore, the splash-dispersed conidia of P. brassicae have an important role in the secondary spread of light leaf spot (McCartney & Lacey, 1990), whereas there is no evidence that the splash-dispersed conidia of L. maculans have a role in spreading the disease in the UK (Hammond & Lewis, 1986). However, the extended period of L. maculans ascospore dispersal means that basal stem canker lesions result from phoma leaf spots on leaves produced at the rosette stage of winter oilseed rape growth in autumn and winter, whereas upper stem lesions result from leaf spots on later leaves.
Fig. 2. Effects of temperature and wetness duration after inoculation on development of phoma leaf spot lesions on oilseed rape leaves (cv. Nickel) inoculated with ascospores of Leptosphaeria maculans. Changes with time in number of lesions on 6 plants (4 leaves per plant); a) at different temperature, with 48 h leaf wetness duration; b) at 20° C with different leaf wetness durations
Evidence from experiments in which fungicides have been used to manipulate development of epidemics suggests that light leaf spot generally decreases yields through killing leaves, and sometimes plants, in winter (Rawlinson et al., 1978; Fitt et al., 1998a), although occasionally flowers and pods are damaged later. By contrast, stem canker decreases yield through damage to stems in spring; when basal cankers or upper stem lesions girdle and kill stems, plants die prematurely and pod and seed development stops (Sansford et al., 1996). Light leaf spot can be particularly damaging in long, cool winters because P. brassicae can continue to infect leaves and sporulate at low temperatures when oilseed rape growth is very slow (Fitt et al., 1998a). However, warm winter weather favours the development of severe stem canker epidemics because L. maculans, with a higher optimum temperature than P. brassicae, can then grow rapidly down petioles to infect stems (Hammond & Lewis, 1986).
FORECASTING SEVERITY OF LIGHT LEAF SPOT AND STEM CANKER
A scheme for forecasting the severity of light leaf spot epidemics (Fitt et al., 1996; Welham et al., 1998) involves regional risk and crop risk forecasts at the beginning of the growing season in October, combined with a protocol for sampling crops to confirm the presence of light leaf spot. Seasonal, regional risk indices, predicting the % crops in a region with light leaf spot in the following March (Fig. 3a), have now been issued in October 1996, 1997 and 1998. In 1998, the forecast was issued as a map showing the risks in different regions of the UK and placed on the world-wide-web (URL http://www.res.bbsrc.ac.uk/molbio/Lls/), so that growers could access it. These regional forecasts are based on survey data collected in the July before they are issued in October. Regional forecasts can now be updated twice during the autumn/winter (in January and February) by addition of factors dependent on autumn rainfall and winter temperature (deviations from 30-year mean values). Spring disease survey data (i.e. March 1997 and 1998) have been used to validate predictions made the previous autumn (i.e. October 1996 and 1997). Observed light leaf spot incidence in spring was never greater than that predicted for a region but was sometimes considerably smaller, perhaps because many crops had been sprayed with fungicide. There is further scope for improving the updating of regional forecasts during the autumn/winter by incorporating factors relating to results of the autumn disease survey and to autumn fungicide use to modify the predicted risk of severe light leaf spot. Regional forecasts have not yet been developed for stem canker, although survey data show that the greatest risks consistently occur in the east and south of England. Furthermore, analyses on eastern region survey data for the period since 1976/77 suggest that rainfall in August/September greatly influences the risk of severe stem canker epidemics (Gladders & Symonds, 1995). Ultimately, there needs to be a forecasting scheme which predicts the risks of severe epidemics of both light leaf spot and stem canker in each region.
Fig. 3. Prediction of light leaf spot risk in October for the following March: a) regional risk, based on survey data from the previous July (% crops in a region with light leaf spot); b) crop risk, based on sowing date, cultivar and ADAS region (Fitt et al., 1996)
Survey data has also been used to investigate how factors, such as cultivar, sowing date and proximity to previous oilseed rape crops, modify the regional risk index to produce specific crop risk indices for individual crops in October (Fitt et al., 1996; Fig. 3b). The aim of these crop risk indices is to provide growers with information about the risks of severe light leaf spot epidemics in their own crops. However, variation in survey data for individual crops has made it more difficult to develop accurate crop risk indices than to develop regional risk indices. Ultimately, there is a need for crop risk indices that can be updated by using information about local weather (e.g. occurrence of infection conditions) and fungicide use and encompass risks of both light leaf spot and stem canker. This information could be incorporated into an interactive world-wide-web site, so that growers can input information themselves to derive modified crop risk indices.
To confirm the presence of light leaf spot in crops with a high predicted risk, a protocol has been developed for sampling crops (which are frequently symptomless in autumn when decisions need to be made) to assess the incidence of the disease (Fitt et al., 1998a). It is suggested that crops are inspected at monthly intervals from October to April, looking for patches of light leaf spot, and sampled by collecting five groups of 20 plants along a diagonal across them. After incubation in polyethylene bags at 10 – 15°C for 3 – 4 days, leaves can be inspected for the presence of the diagnostic white spore pustules of P. brassicae (Fig. 4a) to confirm the presence of the pathogen. To assess the incidence of the phoma leaf spot phase of stem canker in crops in the autumn, it is not necessary to sample or incubate plants since the distinctive spots are clearly visible in the field, from October onwards (Gladders & Musa, 1980). During the period between October and April, it is generally sufficient to assess the % plants with light leaf spot rather than make more time-consuming assessments of light leaf spot severity (Fitt et al., 1998b). Similarly, it should only be necessary to assess the % plants with phoma leaf spot; in theory, one leaf spot can cause one stem lesion/canker of this monocyclic disease and one stem lesion can kill the plant prematurely.
To facilitate accurate diagnosis of light leaf spot when plants are symptomless or display ambiguous symptoms, a molecular method for identification of P. brassicae in infected plants, based on polymerase chain reaction (PCR) amplification to produce a specific 750 base-pair product, has been developed (Foster et al., 1998; Fig. 4b). This product was produced by all P. brassicae isolates tested and by infected leaves, but not by healthy leaves or by other oilseed rape pathogens. However, this diagnostic method can be used only if expensive PCR equipment is available. Further work is being done using molecular methods to identify specific proteins produced in infected leaves as a basis for developing an immunodiagnostic method which can be used by growers. Both molecular and immunodiagnostic methods have also been developed for identification of A-group and B-group isolates of L. maculans in infected plants since composition of the L. maculans population in crops in the autumn affects the risk of severe epidemics (Williams & Fitt, 1999). However, accurate assessment of the incidence of light leaf spot or phoma leaf spot in crops in the autumn depends on the development of accurate methods for sampling plants in crops, based on a knowledge of the spatial distribution of the diseases (Hughes et al., 1996). Further work is also required to relate the observed incidence of light leaf spot or phoma leaf spot in autumn to the severity of light leaf spot or stem canker epidemics in spring and, ultimately, to yield loss.
Fig. 4. Diagnosis of infection by Pyrenopeziza brassicae (light leaf spot) in winter oilseed rape leaves: a) lesions surrounded by characteristic white spore pustules, produced after incubation in a polyethylene bag (Fitt et al., 1998a); b) diagnostic 750 base-pair product produced in a polymerase chain reaction (PCR) using primers specific for P. brassicae (Foster et al., 1998). Lane M, DNA size marker; lanes 1-10, P. brassicae isolates; lane 11, healthy oilseed rape leaf; lane 12, oilseed rape leaf with light leaf spot symptoms; lane 13, negative control
A strategy for integrated management of diseases on winter oilseed rape in the UK currently needs to rely on use of fungicides, since there is no complete resistance to stem canker, light leaf spot, stem rot or dark pod spot in any current cultivars. Cultural practices, such as ploughing in of debris and volunteers from previous oilseed rape crops before emergence of new crops, can help to decrease inoculum sources. Furthermore, there are differences between cultivars in their level of resistance to stem canker and light leaf spot under field conditions (Anonymous, 1997) and growers can select cultivars which are most resistant to the disease which is predominant in their area. More resistant cultivars are likely to require less fungicide treatment; e.g. tebuconazole increased yields of cv. Capitol (rating 8 for resistance to light leaf spot) less than those of cv. Bristol (resistance rating 2) in experiments at Rothamsted where severe light leaf spot developed (Sutherland et al., 1998). Nevertheless, the estimates of losses from diseases of winter oilseed rape (Fig. 1), despite expenditure of up to £12M per season on fungicides (Turner et al., 1999), suggest that there is considerable scope to improve timing of fungicide applications. The survey data suggest that many crops which warranted treatment against stem canker or light leaf spot were not sprayed in autumn and that other crops were sprayed unnecessarily against stem rot or dark pod spot in spring. The results of spray timing experiments and information about the epidemiology of these diseases in the UK suggest that there are three main periods in the growing season when spray decisions need to be made.
1. Autumn. In autumn, decisions need to be taken about application of fungicides to prevent spread of L. maculans from phoma leaf spots to the stem (stem canker) and to eradicate symptomless infections by P. brassicae (light leaf spot) (Fig. 5). The timing of the spray against the phoma leaf spot phase of stem canker is critical, since the pathogen cannot be controlled once it has spread from the leaf to the stem. Poor control has been achieved by sprays applied too early in some years, or too late in others (Gladders et al., 1998). Whilst survey results already indicate that the greatest risks of severe stem canker epidemics are in the east and south, there is a need to develop regional forecasts to quantify the risks in each region more accurately. To improve the timing of sprays against stem canker, it is necessary to develop methods for predicting the time when incidence of phoma leaf spot increases rapidly (which varies between seasons and sites from early October to late November; Biddulph et al., pers. comm.). Recent research has shown that this increase in incidence of phoma leaf spot cannot easily be related to peaks in numbers of air-borne L. maculans ascospores (West et al., 1998) or to occurrence of weather favourable for infection (Biddulph et al., 1998). It seems likely that, as in France (Pérès & Poisson, 1997), differences between seasons and sites in timing of leaf spotting may be related to differences in factors affecting maturation of ascospores, such as rainfall in August/September (Gladders & Symonds, 1995). Thus, there is a need to test whether the weather-based CETIOM model (Pérès & Poisson, 1997) for describing ascospore maturation can be used to improve timing of sprays against stem canker in the UK.
Fig. 5. Times (arrows) at which decisions need to made about application of fungicides to UK winter oilseed rape, in relation to typical disease progress curves of: a) stem canker (Leptosphaeria maculans); b) light leaf spot (Pyrenopeziza brassicae); c) stem rot (Sclerotinia sclerotiorum); d) dark pod spot (Alternaria brassicae). Modified from Fitt et al. (1997)
In autumn, growers in Scotland and the north and west of England need to be more concerned about the risk of severe light leaf spot epidemics than about stem canker. The regional light leaf spot forecasts can help to guide their decisions (Welham et al., 1998). There is a need to extend these regional forecasts to Scotland and to introduce crop risk forecasts in a form that can be used by growers. The optimum timing for spraying against the phoma leaf spot phase of stem canker is often in October but for spraying against light leaf spot it is often in November. Growers in areas at risk from both diseases may need to compromise their spray timing, although the timing of sprays against stem canker is often more critical than timing of sprays against light leaf spot (Gladders et al., 1998; Sansford et al., 1996).
2. Late winter/early spring (stem extension). There is a need to reassess the risk of severe stem canker or light leaf spot in late winter/early spring, since severe epidemics of either disease cannot be controlled by a single fungicide spray (Fitt et al., 1997). Generally, two half-dose applications of fungicide, in autumn and late winter, provide better disease control and produce better yield responses than a single full-dose spray in autumn or late winter. The second spray provides control of the phoma leaf spots which produce the upper stem lesions and against an increase in epidemic development of the polycyclic light leaf spot. The yield loss model of Su et al. (1998), based on % plants with light leaf spot in the crop, can be used to assess the risk of severe light leaf spot at this stage and observation of phoma leaf spotting can help decisions about a further spray against stem canker. The updated regional light leaf spot forecasts, based on winter weather, can also be considered, but there is a need to develop reliable regional risk and crop risk forecasts, combined for light leaf spot and stem canker, which can be updated in the late winter/early spring.
3. Spring (flowering). A single, well-timed spray during flowering (GS 4,5) can prevent the establishment of Sclerotinia sclerotiorum in fallen petals on leaves and development of stem rot (Davies, 1995). Methods developed for assessing the risk of severe stem rot epidemics, based on previous incidence of stem rot, were greatly improved by applying a scheme for culturing fallen petals sampled from crops to assess the presence of S. sclerotiorum. These methods confirmed that many crops are sprayed unnecessarily against stem rot, since the coincidence of petal fall, S. sclerotiorum ascospore release and wet weather required for stem rot development rarely occurs in the UK. Similarly, single post-flowering (95% petal fall) sprays can provide good control of dark pod spot (Gladders, 1988) and the pod phase of light leaf spot but are rarely necessary in the UK. Since lodging favours the development of dark pod spot, avoidance of excessive seed rates at sowing or excessive rates of nitrogen fertiliser can help to minimise risk of dark pod spot epidemics. Decisions about the need for control of dark pod spot can be based on observations of disease in the crop and occurrence of weather favourable for dark pod spot development in May (Hong et al., 1996; Kennedy et al., 1995).
Surveys suggest that the incidence of light leaf spot in England and Wales has decreased since 1995 (Fig. 1), as the proportion of crops sprayed in autumn has increased (Turner, pers. comm.), suggesting that the light leaf spot forecasting scheme has helped to improve farming practice. However, there is still much scope for work to improve timing of sprays against stem canker, and to decrease unnecessary application of sprays against stem rot or dark pod spot. Ultimately, there is a need to construct a decision support system for integrated management of diseases in winter oilseed rape in the UK. However, such a decision support system can be reliable and robust only if it is based on accurate understanding and accurate models of the epidemiology of the important diseases. The priorities now must be to obtain accurate biological data about the development of stem canker, to construct accurate models to describe these data, and to develop combined regional risk and crop risk forecasts for light leaf spot and stem canker.
This work was funded by the UK Ministry of Agriculture, Fisheries and Food, the Biotechnology and Biological Sciences Research Council, the Home-Grown Cereals Authority, the Scottish Office, the European Union, the Perry Foundation and Bayer PLC. We thank J.E. Biddulph, N. Castells-Brooke, S.J. Elcock, S.J. Foster, T. Gilles, P.K. Leech, C.E. Sansford, S. Souter, J.M. Steed, B.V. Symonds, J.S. West and other colleagues for their contribution to the work.
1. Anonymous (1997). UK recommended list of oilseeds 1997. National Institute of Agricultural Botany, Cambridge. 7pp.
2. Ansan-Melayah, D., Rouxel, T., Bertrandy, J., Letarnec, B., Mendes-Pereira, E. & Balesdent, M.H. (1997). Field efficiency of Brassica napus specific resistance correlates with Leptosphaeria maculans population structure. European Journal of Plant Pathology 103, 835-841.
3. Ashby, A.M. (1997). A molecular view through the looking glass: the Pyrenopeziza brassicae – Brassica interaction. Advances in Botanical Research 24, 32-70
4. Biddulph, J.E., Fitt, B.D.L. & Welham, S.J. (1998). Effects of temperature and wetness duration on infection of oilseed rape leaves by ascospores of Leptosphaeria maculans (stem canker). Abstract 2.5.13, 7th International Congress of Plant Pathology, Edinburgh.
5. Davies, J.M.L. (1995). Petal culturing to forecast Sclerotinia in winter oilseed rape. Proceedings of 9th International Rapeseed Congress, Cambridge, 1011-1012.
6. Figueroa, L., Shaw, M.W., Fitt, B.D.L., McCartney, H.A. & Welham, S.J. (1994). Effects of previous cropping and fungicide timing on the development of light leaf spot (Pyrenopeziza brassicae), seed yield and quality of winter oilseed rape (Brassica napus). Annals of Applied Biology 124, 221-239.
7. Figueroa, L., Fitt, B.D.L., Welham, S.J., Shaw, M.W. & McCartney, H.A. (1995). Early development of light leaf spot (Pyrenopeziza brassicae) on winter oilseed rape (Brassica napus) in relation to temperature and leaf wetness. Plant Pathology 44, 641-654.
8. Fitt, B.D.L., Gladders, P., Turner, J.A., Sutherland, K.G. & Welham, S.J. (1996). Predicting risk of severe light leaf spot (Pyrenopeziza brassicae) on winter oilseed rape in the UK. 1996 Brighton Crop Protection Conference – Pests and Diseases, 239-244
9. Fitt, B.D.L., Gladders, P., Turner, J.A., Sutherland, K.G., Welham, S.J. & Davies, J.M.L. (1997). Prospects for developing a forecasting scheme to optimise use of fungicides for disease control on winter oilseed rape in the UK. Aspects of Applied Biology 48, 135-142.
10. Fitt, B.D.L., Doughty, K.J., Gladders, P., Steed, J.M. & Sutherland, K.G. (1998a). Diagnosis of light leaf spot (Pyrenopeziza brassicae) on winter oilseed rape (Brassica napus) in the UK. Annals of Applied Biology 133, 155-166.
11. Fitt, B.D.L., Doughty, K.J., Gilles, T., Gladders, P., Steed, J.M., Su, H. & Sutherland, K.G. (1998b). Methods for assessment of light leaf spot (Pyrenopeziza brassicae) on winter oilseed rape (Brassica napus) in the UK. Annals of Applied Biology 133, 329-342.
12. Foster, S.J., Ashby, A.M. & Fitt, B.D.L. (1998). Molecular diagnosis of light leaf spot (Pyrenopeziza brassicae) on winter oilseed rape. IOBC Bulletin 21, 235-239.
13. Gladders, P. (1988). The contribution and value of pesticides to disease control in combinable break crops. In: Control of Plant Diseases: Costs and Benefits, pp. 29-50. Eds. B.C. Clifford & E. Lester. Oxford: Blackwell Scientific Publications.
14. Gladders, P. & Musa, T.M. (1980). Observations on the epidemiology of Leptosphaeria maculans stem canker in winter oilseed rape. Plant Pathology 44, 641-654.
15. Gladders, P. & Symonds, B.V. (1995). Occurrence of canker (Leptosphaeria maculans) in winter oilseed rape in Eastern England, 1977-1993. IOBC Bulletin 18, 1-11.
16. Gladders, P., Symonds, B.V., Hardwick, N.V. & Sansford C.E. (1998). Opportunities to control canker (Leptosphaeria maculans) in winter oilseed rape by improving spray timing. IOBC Bulletin 21, 111-120.
17. Hammond, K.E. & Lewis, B.G. (1986). The timing and sequence of events leading to stem canker disease in populations of Brassica napus var. oleifera in the field. Plant Pathology 35, 551-564.
18. Hammond, K.E., Lewis, B.G. & Musa, T.M. (1985). A systemic pathway in the infection of oilseed rape plants by Leptosphaeria maculans. Plant Pathology 34, 557-565.
19. Hardwick, N.V. & Turner, J.A. (1994). Fungicide use on winter oilseed rape in England and Wales, 1986-1993. 4th International Conference on Plant Diseases, Bordeaux. ANPP, 1163-1170.
20. Hong, C.X., Fitt, B.D.L.& Welham, S.J. (1966). Effects of wetness period and temperature on development of dark pod spot (Alternaria brassicae) on oilseed rape (Brassica napus). Plant Pathology 45, 1077-1089.
21. Hughes, G. Madden, L.V.& Munkvold, G.P. (1996). Cluster sampling for disease incidence data. Phytopathology 86, 132-137.
22. Kennedy, R. & Graham, A.M. (1995). Infection of oilseed rape by Alternaria brassicae under varying conditions of temperatures and wetness. Proceedings of 9th International Rapeseed Congress, Cambridge, 601-603.
23. McCartney, H.A. & Lacey, M.E. (1990). The production and release of ascospores of Pyrenopeziza brassicae on oilseed rape. Plant Pathology 39, 17-32.
24. Majer, D., Lewis, B.G. & Mithen, R. (1998). Genetic variation among field isolates of Pyrenopeziza brassicae. Plant Pathology 47, 22-28.
25. Paul, V.H.& Rawlinson, C.J. (1992). Diseases and Pests of Rape. Verlag Th. Mann, Gelsenkirchen-Buer, Germany. 132 pp.
26. Pérès, A. & Poisson, B. (1997). Phoma du colza: avancées en epidemiologie. CETIOM – Oléoscope 40, 37-40.
27. Rawlinson, C.J., Muthyalu, G., Cayley, G.R. (1984). Fungicide effects on light leaf spot, canker, crop growth and yield of winter oilseed rape. Journal of Agricultural Science, Cambridge 103, 613-628.
28. Rawlinson, C.J., Sutton, B.C. & Muthyalu, G. (1978). Taxonomy and biology of Pyrenopeziza brassicae sp. nov. (Cylindrosporium concentricum), a pathogen of winter oilseed rape (Brassica napus ssp. oleifera). Transactions of the British Mycological Society 71, 425-439.
29. Sansford, C.E., Fitt, B.D.L., Gladders, P., Lockley, K.D. & Sutherland, K.G. (1996). Oilseed rape: disease development, forecasting and yield loss relationships. Home-Grown Cereals Authority Project Report OS 17. 185 pp.
30. Su, H., Fitt, B.D.L., Welham, S.J., Sansford, C.E. & Sutherland, K.G.(1998). Effects of light leaf spot (Pyrenopeziza brassicae) on yield of winter oilseed rape (Brassica napus). Annals of Applied Biology 132, 371-386.
31. Sutherland, K.G., Fitt, B.D.L., Steed, J.M., Welham, S.J., Gladders, P. & Turner, J.A. (1998). Development and control of light leaf spot (Pyrenopeziza brassicae) epidemics in winter oilseed rape in the UK. 1998 Brighton Crop Protection Conference – Pests and Diseases, 1053-1058.
32. Sutherland, K.G., Wale, S.J., Sansford, C.E. (1995). Effect of different epidemics of Pyrenopeziza brassicae on yield loss in winter oilseed rape. Proceedings 9th International Rapeseed Congress, Cambridge, 1004-1006.
33. Sylvester-Bradley, R. & Makepeace, R.J. (1985). Revision of a code for stages of development in oilseed rape (Brassica napus L.). Aspects of Applied Biology 10, 395-400.
34. Turner, J.A., Gladders, P., Elcock, S.J., Walters, K.F.A.& Wright, D.M. (1999). Winter oilseed rape: survey of pests and diseases, 1997/98. CSL/ADAS Research and Development, York. 57 pp.
35. Welham, S.J., Turner, J.A., Fitt, B.D.L., Gladders, P. & Sutherland, K.G. (1998). Empirical models for prediction of regional light leaf spot (Pyrenopeziza brassicae) incidence on winter oilseed rape in the UK. Abstract 2.1.9, 7th International Congress of Plant Pathology, Edinburgh.
36. West, J., Leech, P. & Fitt, B.D.L. (1998). The effects of rainfall on numbers of air-borne ascospores of Leptosphaeria maculans and the development of phoma leaf lesions on winter oilseed rape. Abstract 2.1.7, 7th International Congress of Plant Pathology, Edinburgh.
37. Williams, R.H. & Fitt, B.D.L. (1999). Differentiating A and B groups of Leptosphaeria maculans, causal agent of stem canker of winter oilseed rape in the UK – a review. Plant Pathology 46 (in press).