Integration of environmental and fungicidal control of Bremia lactucae in a glasshouse lettuce crop

CROP PROTECTION (1984) 3 (2), 349-361

Integration of environmental and fungicidal control of Bremia lactucae in a glasshouse lettuce crop WALTER M. MORGAN~

Glasshouse Crops Research Institute, Littlehampton, West Sussex, BN16 3PU, UK ABSTRACT. The effect of combinations of night ventilation regimes and fungicide treatments on levels of downy mildew (Bremia lactucae) was investigated in a November-sown glasshouse lettuce crop. Environmental regimes were allocated in a randomized-block design to glasshouse compartments in which fungicide treatments were applied to sub-plots from which sub-sub-plots were harvested on each of four dates. The benefit of night ventilation was strikingly shown. It was almost as effective as the systemic fungicide metalaxyl which gave complete control of B. lactucae for 20 weeks after its incorporation in the peat blocks. A 'heat-purging' treatment increased the incidence of downy mildew, while other fungicidal regimes failed to control late infection. In the period close to cutting, when fungicide usage is not permitted, night ventilation may be the only effective means of controlling the disease.

Introduction Conventional methods of controlling B. lactucae on lettuce under glass are by manipulation of the heating and ventilation system, by growing resistant cultivars and by fungicides (Anonymous, 1980). There are problems with these methods of control. Because conidia of the fungus will germinate only in free water (Verhoeff, 1960), the leaves must be kept as dry as possible if the crop is to remain free from downy mildew. However, monitoring and control of free water on lettuce is difficult because of the closely adpressed leaves of the adult plant. Monitoring and control of atmospheric humidity is more feasible. However, techniques of achieving this control by heating and ventilating tend to be based on anecdotal rather than on experimental evidence. As fuel costs rise, so the trend is for growers of heated crops to restrict ventilation, especially at night, and to save energy by a variety of other techniques. All these methods of saving fuel cause increases in the humidity of the air (Morgan, 1982). T h e effectiveness of resistant cultivars is liable to be nullified by new virulent *Present address: Twyford Plant Laboratories, Baltonsborough, Glastonbury, Somerset, BA6 8QG,

UK. 0261-2194/84/03/0349-13503.00 © 1984Butterworth & Co (Publishers)Ltd

350

Control ofBremia lactucae in glasshouse lettuce

races selected from the pathogen population (Crute and Johnson, 1976). Also, in recent years, chemical control of B. lactucae has been in a state of flux because of (1) the restricted use of dithiocarbamate fungicides (e.g. zineb) to reduce residues at harvest (Griffin and Griffin, 1977) and (2) the threat of insensitivity in the fungus toward the highly effective and widely-used metalaxyl (Crute and Jagger, 1979). It is therefore unwise to rely on a resistant cultivar or a downy mildew specific fungicide alone. As suggested by Wolfe (1981), an integrated programme using diverse elements of control is likely to be more durable. Thus, alternative methods of disease control are important and more precise methods of environmental control would be beneficial. Pathologists interested in diseases of protected crops intuitively accept that control of disease by environmental manipulation is worth while, although there is little experimental evidence of its effectiveness i n comparison with chemical methods of disease control. Lettuce demands a cool environment and has a low market value which restricts the use of additional heating to lower air humidity. Nevertheless, as part of their strategy of disease control, lettuce growers use combinations of heating to 20-25°C and ventilation (heat purging), or ventilation alone, in an attempt to prevent the humidity rising while air temperatures fall after sunset (Large, 1972; Crute and Dixon, 1981). This experiment was designed to compare the effects of the most energyconsumptive regime (continuous night ventilation) with the most energy-conservative (no night ventilation) and with a compromise based on the heat-purging technique (heating and ventilation at dusk only). The experiment also examines interactions and comparisons between the environmental treatments and the most effective fungicides in use at the time of the experiment in 1979, i.e. the systemic fungicides metalaxyl and phosetyl-aluminium and the alternative protectant chemical, zineb. Methods Crop

Nine unheated Cambridge Alumabrite glasshouse compartments (9-75 x 6-25 m) were used for the experiment. Pelleted seed (cv. Amanada Plus) were sown in 4"3 cm peat blocks on 10 November. In the propagation glasshouse, a minimum air temperature of 15-5°C was maintained until seedlings emerged, after which they were raised at minimum temperatures of 13°C (day) and 7°C (night). Throughout propagation, the maximum temperature was regulated by automatic ventilation at 18.5°C. The peat blocks were planted to about half their depth, at 20 x 20 cm spacing in nine glasshouse compartments on 14 December, by which time the seedlings had two true leaves. They were planted in five sub-plots in each compartment with two guard rows at each gable end (Figure 1). For the first 2 weeks after planting, minimum air temperatures were maintained at 13°C (day) and 7°C (night), and thereafter at 7°C (day) and 4-5°C (night), with ventilators opening at 18"5°C. The crop was cut for market between 22 and 30 March. Environmental treatments

The three night ventilation treatments were: 1.

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351

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FIGURE 1. Randomized block design with split-split-plots used in an experiment to test the interactions of environmental regimes with fungicidal treatments in the control of lettuce downy mildew in three compartmented glasshouses. Examples of randomization of fungicide treatments and harvest dates are shown.

2. 3.

18.5°C. Therefore, due to the low ambient temperatures in winter, the ventilators effectively remained closed throughout the night. Ventilators kept open about 7-5 cm on both sides (lee side only when windy) between dusk and dawn. A 'heat-purging' regime. Starting one hour before sunset, ridge ventilators were opened for 30 min, followed by 30 min heating with ventilators closed, then a further 30 min ventilation. The ventilators were then closed until dawn.

Each treatment was allocated randomly to one of the three compartments in each of the three statistical blocks (Figure 1).

Environmental monitoring Glasshouse air temperature and relative humidity (r.h.) were monitored using Casella bimetallic/hair thermohygrograph recorders mounted in aspirated screens sited centrally in each compartment at a height of 1-2 m above soil level. The sequence of ventilation/heat/ventilation used in the 'heat-purge' regime caused a peak of temperature and a corresponding abrupt trough in r.h. of about 30 min

352

Control ofBremia lactucae in glasshouse lettuce

duration at dusk. T h e mean m a x i m u m t e m p e r a t u r e attained was 21.3°C and the mean m i n i m u m r.h. was 53-2%. T h e mean t e m p e r a t u r e and r.h. during each night was estimated to the nearest 0.5°C and 5~o, respectively, and the frequency of these m e a s u r e m e n t s in each environmental treatment is shown in T a b l e 1. T h e most frequent mean night t e m p e r a t u r e was 5.5°C in all treatments. Ventilation at night prevented mean temperatures from rising above 9°C. T h e environmental treatments appeared to cause differences in r.h. at night: the most frequent humidity category in the ventilated, unventilated and heat-purged treatments were 85, 90 and 95%, respectively. H e a t purging also caused a high frequency of nights with mean r.h. >97%. TABLE 1. The effect of three environmental regimes on mean relative humidity and mean temperature at night in a glasshouse lettuce crop Temperature ~ (°C) and relative humidity ~

Environmental regime

(%)

Ventilated Unventilated 'Heat-purged'

Relative humidity (approximated to nearest 5%) >97 1 95 49 90 55 85 57 8O 41 75 27 70 7 65 2 60 1 Temperature (approximated to nearest 0.5°C) 11 0 10"5 0 10 0 9"5 0 9 5 8"5 3 8 12 7"5 12 7 8 6"5 41 6 43 5"5 69 5 41 4"5 4

0 59 78 58 23 8 3 2 0

26 92 54 49 13 9 2 0 0

1 2 6 0 3 6 8 14 10 12 58 100 19 2

0 0 2 3 8 6 4 11 11 19 53 71 37 6

* The total number of nights between planting and cutting, in three replicate compartments with the given mean temperature or humidity are listed.

WALTERM. MoRGAN

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Fungicide treatments The four fungicide treatments were: i.

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Metalaxyl (methyl-N-(2-methoxyacetyl)-N-2,6-xylyl)-nL-alaninate, 50 g (a.i.)/m 3 uncompressed peat) incorporated into the peat blocks before seed sowing as 40 g Ridomil (25% w.p.) per 200 Y bale. Phosetyl-aluminium (aluminium tris (ethyl phosphonate), 480 g (a.i.)/m 3 uncompressed peat) incorporated into the peat blocks before seeds were sown as 120 g Aliette (80% w.p) per 200 d bale. Zineb (zinc ethylenebis (dithiocarbamate), 1-4 g (a.i.)/() applied as a spray to run-off four times before planting, on 17, 24 November and 1, 8 December and twice after planting, on 18 December and 5 January. Untreated.

Each fungicide treatment and two replicates of the untreated control were allocated randomly to one of the five sub-plots within each glasshouse compartment (Figure

1). All plants were routinely sprayed with seven applications of iprodione to run-off (3-(3,5-dichlorophenyl)-N-isopropyl-2,4-dioxoimidazolidine-l-carboxamide, 0-5 g (a.i.)/(; as Rovral 50% w.p.) to control infection by Botrytis cinema Pers. ex Ft.

Inoculation with Bremia lactucae By mid-February, downy mildew infection from natural inoculum was not apparent and, therefore, inoculum of B. lactucae was introduced into each glasshouse. An isolate (virulence genes 1, 2 and 6) was maintained on lettuce seedlings cv. Southdown using the methods described by Morgan (1983). Two weeks after sowing seed in 5 cm pots of peat:sand:John Innes compost No. 1 (1:1:2), the seedlings were thinned to one per pot and inoculated by spraying with a suspension of conidia (c. 105/ml), enclosed in bags overnight and returned to the illuminated bench for a further 7 days. They were then again enclosed in bags overnight to encourage sporulation and transferred to the glasshouses the following evening where the bags were removed. One potted infected seedling was supported on the aspirated screen, in the centre of each glasshouse compartment, at a height of 1-45 m on 17 February and replaced on 23 February and 1 and 12 March. Downy mildew was first observed in the plots on 16 March.

Cutting and yield assessment The crop was cut, and yield and disease assessments made on 22, 26, 28 and 30 March (harvests 1-4, respectively). In each sub-plot assessments were made on all 100 plants which were surrounded by a single row of guard plants. Harvest dates were allocated randomly to quarters (sub-sub-plots, each of 25 plants) of each sub-plot: randomization was restricted so that the first and second harvests were not taken from diagonally opposite quarters, to even out competition between sub-sub-plots within each sub-plot in the intervals between harvest dates. Plants were cut, trimmed, graded and weighed. The yield variates collected from each sub-sub-plot were: total weight of the plants at cutting; number of plants of marketable quality; total marketable weight; and the mean weight of the marketable plants.

354

Control ofBremia lactucae in glasshouse lettuce

Disease assessment

After cutting, and before trimming, the number of leaves infected with downy mildew was counted on each plant. The trimmings, leaves and basal tissue removed to make the base of the plant and the wrapper leaves clean and free from disease, were bulked from each sub-sub-plot. They were then segregated into leaves with or without downy mildew and the weight of each sub-sample recorded. Trimming losses attributable to other pathogens were very rare and were considered to be negligible. The disease variates collected from each sub-sub-plot were: total number of infected leaves; total number of infected plants; weight of trimmings infected with downy mildew; and the weight of trimmings apparently not infected with B. lactucae. Data analysis

All data were analysed by the analysis of variance (ANOVA) technique. Where data were not cumulated, they were analysed at each of the four harvest dates. To satisfy the assumptions of the ANOVA technique, disease and trimming data were transformed to the square root scale before analysis. For ease of interpretation means have been transformed back to the original scale. Arcsine transformation of counts of diseased plants did not improve the precision of the analysis. Because metalaxyl gave complete control of the disease, it was excluded from the analysis of disease variates. Yield data were analysed without transformation. Treatment means from the same harvest were compared using the least significant difference (LSD; P = 0"05 and 0-1); standard errors of treatment means (SE) are shown in the Figures. A positional effect was detected in the sub-plot treatments caused by proximity to the glasshouse doorway; lettuce were lighter in sub-plots closer to the doorway, but had less disease. This was assumed to be due to increased ventilation at the doorway causing a local micro-climate gradient with lower temperatures and lower humidities. Although the use of a co-variate eliminated the effect, especially in the early harvests while disease levels were low, it did not improve the precision of treatment comparisons. Results presented are based on data not adjusted for the co-variate. As a result of an unexpectedly high number of unmarketable plants from one glasshouse, the variability was too large to justify analysis of variance of the number of marketable plants or of the total marketable weight. Results Disease and crop loss Infected leaves. Plants grown with night ventilation had substantially reduced numbers of infected leaves compared with plants grown with the ventilators closed or with heat-purging (Figure 2a); these differences were statistically significant from harvest 2 onwards. Heat-purged plants had more infected leaves than unventilated plants but numbers were not significantly different. Metalaxyl completely controlled the disease. Although plants with the other fungicide treatments had less infection than the untreated plants, the only significant difference was between zineb-treated and untreated plants at harvest 2. The glasshouse environment greatly influenced disease levels (Table 2). Plants

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metalaxyl • . . . . . • ; phosetyl-A1D-.-.-.E]; zineb # . . . . . . #; untreated zx zx) on (a) number of lettuce leaves infected with B. lactucae, (b) the incidence of infected plants and (c) the weight of trimmings with and without symptoms of B. lactucae infection at four harvest dates• Data are means derived from analyses excluding the metalaxyl treatment (except in (c), 'without symptoms'), using a square-root transformation. T h e y are plotted on a l i n e a r square-root scale, with the ordinate axis back-transformed. Bars are SE; shorter solid bar is used for comparisons made between 'untreated' and a fungicide treatment.

356

Control ofBremia lactucae in glasshouse lettuce TABLE2. The influence of the glasshouse environment on the effectiveness of fungicides for the control of B. lactucae on lettuce. Mean number of infected leaves per plant over four harvests Environment Treatment Untreated Zineb Phosetyl-aluminium Metalaxyl

Unventilated Ventilated Heat-purged 2-60a 1.00b 1.12a 0-00

0.28 0.20 0"16 0.00

2.37 a 2-24a 3.16~ 0.00

These figures are back-transformed means, derived from ANOVA using a square-root transformation and excluding the metalaxyl treatment. Responses significantly different from zero are denoted by a or b (confidence interval does not include zero) P = 0'05 and 0' 1, respectively. grown with ventilation at night and without fungicides had such low levels of disease that the benefit of applying fungicides was questionable. This was not the case in unventilated or heat-purged glasshouses where disease levels were high and the benefits of metalaxyl treatment were obvious.

Infected plants. T h e unventilated and heat-purged treatments allowed a significantly greater level of infection than did ventilation at harvests 2, 3 and 4 (Figure 2b). T h e r e was no significant difference between the heat-purged and unventilated treatments. T r e a t m e n t with zineb significantly reduced the n u m b e r of infected plants in comparison with the untreated control at harvests 1 and 2. Therefore, the pattern of response to the treatments of numbers of infected plants was generally the same as that o f counts of infected leaves. This indicates that infected leaves were evenly distributed over infected plants within each treatment. Trimming losses. T h e response of the weight of infected trimmings to the environmental and fungicidal treatments was similar to the other parameters of disease (Figure 2c); the unventilated plants produced significantly more infected trimmings at harvest 1 than did the heat-purged and the ventilated plants. T h e r e were no other statistically significant differences in trimmings with symptoms between either the environmental or the fungicidal treatments. Weights of trimmings without symptoms of B. lactucae infection were much larger than those with symptoms (Figure 2c). T h u s the visibly infected trimmings alone do not give a true measure of the loss due to downy mildew. T h e r e were significantly greater weights of trimmings without symptoms from unventilated and heat-purged plants than from ventilated plants at harvest 2. Plants treated with metalaxyl produced significantly less trimmings without symptoms than did untreated plants at every harvest, less than zineb and phosetyl-aluminium treatment at harvest 3 and less than zineb at harvest 4. Zineb-treated plants had significantly less symptomless trimmings than untreated plants at harvest 2 alone. Lettuces from the ventilated and

WALTERM. MORGAN

357

metalaxyl treatments, which had little or no disease, produced very similar weights of trimmings (Figure 2c), i.e.c. 6 g/plant at harvest 1, rising to c. 24 g/plant at harvest 4. There was a direct relationship between losses due to trimmings, with and without symptoms, and the disease incidence, i.e. high levels of downy mildew caused greater trimming losses, both infected and uninfected. These uninfected trimmings were not damaged by other pathogens, but were healthy leaves removed, together with leaves infected with downy mildew, by trimming the plant transversely across the base.

Yield Marketable plants. A substantial proportion of the plants from the heat-purged treatment could not be sent to market at harvest 4 (Figure 3a). With the exception of plants treated with metalaxyl, substantial losses in marketable plants also occurred in response to fungicide treatments, especially at harvest 4 (Figure 3a). Mean weight of marketable lettuce. By harvest 3, the mean weight of the marketable plants from the ventilated treatment was higher than that from the other environmental treatments (Figure 3b). At harvest 4, marketable ventilated plants were on average c. 8 g and 16 g heavier than plants from the unventilated and heat-purged treatments, respectively. Of the fungicide treatments, only metalaxyl allowed the plants sent to market to increase linearly in weight at each harvest. The other treatments were approaching their maximum marketable weight by harvest 3, and at harvest 4, metalaxyl-treated plants were significantly heavier than those treated with zineb or untreated. The response in weight of marketable plants to treatment with metalaxyl was strikingly similar to the response of plants to night ventilation. Weight at cutting. There was a linear increase in weight at cutting from the three environmental treatments but no statistically significant differences between treatments (Figure 3c). Metalaxyl treated plants had the lowest weights at cutting. Because a detectable loss in weight due to infection per se is unlikely so close to maturity, this parameter possibly indicates phytotoxic effects of the fungicide treatments. Total marketable weight. Differences in the total weight of marketable produce in response to environmental treatment were detected in the second and subsequent harvests, in which the ventilated treatment gave the highest yield (Figure 3c). Without night ventilation, there was no change in the total weight of the marketable plants after harvest 3. Yields from heat-purged plants reached a maximum at harvest 3 then fell at harvest 4 to a weight similar to that from harvest 1. In response to fungicides, the total marketable weight continued to rise linearly only where plants had been treated with metalaxyl. In all the other treatments, the yield reached a maximum by harvests 2 or 3, then fell. Productivity andyield losses. The differences between the weight at cutting and the weight marketed (Figure 3c) represent the total loss in weight and clearly

Control ofBremia lactucae in glasshouse lettuce

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FIGURE 3. T h e influence of the glasshouse environment (left; ventilators closed • •; ventilators open O . . . . . O; heat-purged A-.-.-. J,) and fungicide treatments (right; metalaxyl • . . . . . I ; phosetyl-A1 n-.-.-.D; zineb * ...... *; untreated zx z~) on (a) the yield of plants of marketable quality, (b) the mean weight of lettuce of marketable quality and (c) the weight of lettuce at cutting and the total weight of plants of marketable quality at four harvest dates. Bars are SE; the shorter solid bar is used for comparisons between 'untreated' and a fungicide treatment. In (c) the SE bars are derived from the 'weight at cutting' data only.

WALTERM. MORGAN

359

demonstrate a correlation with disease level. It is of interest that in graphs of total weight marketed (Figure 3c) and mean weight of marketable lettuce (Figure 3b), those treatments which controlled the disease best, i.e. metalaxyl and night ventilation, had comparatively low weights at harvest 1 when disease levels were low, possibly because treatments were slightly phytotoxic, but by harvest 4, when disease levels were high, these treatments had the highest weights. A comparison at harvest 4 of yield and weight losses in plants with and without ventilation at night is shown in Table 3. Plants grown with ventilation were lighter at cutting, but heavier when trimmed for market because less leaf and basal tissue was removed to make the plants saleable. However, overtly diseased trimmings were only a small proportion of the total waste material. TABLE 3. Mean weight (g/plant) at the final harvest and yield loss in glasshouse lettuce grown with or without night ventilation Environment Unventilated Ventilated Untrimmed head (all plants) Trimmed head (marketable plants)t Undiseased trimmings (all plants) Diseased trimmings (all plants)~

230"4 190.5 40"5 2.0

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~"Does not include lettuce unfit for market. Infected with B. lactucae.

Discussion This experiment demonstrates very clearly the importance of ventilation in the control of downy mildew in protected lettuce crops, especially in the period before cutting, when certain chemicals may not be applied to the crop for fear of high residues. Chemical and environmental methods of disease control have rarely been compared. Metalaxyl has been found in a number of studies to be one of the most effective chemicals to be used on a commercial scale against downy mildews (Smith, 1979). In this study, night ventilation and metalaxyl were found to be strikingly similar in their effectiveness. Growers may increase their use of chemical fungicides because, in order to save fuel, they have made the glasshouse environment more conducive to disease. This may be a cost-effective, but short-sighted strategy because it will increase the selection pressure towards the development of insensitive strains and provide an environment favourable to their establishment in the crop. Hence the useful life of fungicides may be shortened. One such chemical, under threat, is metalaxyl, to which insensitivity has developed in other oomycete pathogens, e.g. Phytophthora infestans (Cooke, 1981), Peronospora hyoscyami (Bruck, Gooding and Main, 1982) and Pseudoperonospora

360

Control ofBremia lactucae in glasshouse lettuce

cubensis (Reuveni, Eyal and Cohen, 1980), but which is still generally effective in the control of downy mildew of lettuce. To reduce the selection pressure on pathogens, formulations of metalaxyl alone have been replaced with a mixture containing metalaxyl plus mancozeb. A more effective 'back-up' combination of treatments would be metalaxyl plus night ventilation, but this would transfer control of the safeguard from the chemical manufacturer to the grower. The loss of metalaxyl through the development of insensitivity in B. lactucae would leave lettuce growers without an effective means of chemical control. They should therefore be conscious of this when making decisions about ventilation in glasshouse lettuce crops. This experiment also shows the crucial importance of the environment in trials of fungicide effectiveness under glass. Generally, a range of environments is not used because of constraints on space. Whether or not to ventilate is a dilemma in planning a fungicide trial. Is it better to impose conditions which will favour disease or to impose conditions more similar to those used in commercial production? Under the conditions of this experiment, on lettuce grown in a regime which allowed night ventilation, there was no justification for applying fungicides. Zineb, restricted to two sprays after planting (to prevent high residues), was relatively ineffective against late infection, which probably confirms the presence of meagre residues of zineb on the foliage. Similarly, phosetyl-aluminium failed to control the pathogen, presumably because the active ingredient was insufficiently persistent in the blocking compost and had become depleted by the time of infection. Heat-purging was not an effective means of control of downy mildew. Rather, levels of mildew were higher than in unventilated glasshouses and this was probably attributable to higher humidities during the night. The increase in humidity and consequently in mildew may be due to the rise in temperature during the heating phase of the purge. High temperature may increase the rate of transpiration at night; it may also change the leaf morphology and increase susceptibility to infection by B. lactucae (Crute and Dixon, 1981). If the build-up of humidity at dusk is significant in the epidemiology of downy mildew in lettuce, then it should probably be alleviated with ventilation alone and not heat. There was some indication that night ventilation and metalaxyl, which gave best control of downy mildew, were also 'phytotoxic'. Plants sent to market were consequently slightly lighter from early harvests, but at later harvests when disease levels were higher, losses due to removal of infected material in other treatments were much greater than losses due to phytotoxicity. Although small lettuce may be downgraded in quality and value, the weight loss due to phytotoxicity was too small to affect quality, whereas the losses due to disease undoubtedly did affect marketability. Thus the risk to crop yield and quality of applying a prophylactic but phytotoxic treatment is low, should subsequent levels of disease be low. Conversely, the benefit is high should disease be severe. The experiment shows the progress of an epidemic in which the increase in disease is probably not due to spread of infection from one plant to another; rather, it demonstrates variability in the time of infection and length of the latent period. Thus, plants going to market from harvest 1 would certainly have leaves which appeared healthy but which, in the environment of a polyethylene bag, would later show symptoms of downy mildew. Therefore, plants from treatments which controlled the disease poorly are likely to be rejected by the consumer. Thus in the period before harvest, when the use of chemicals is prohibited, infection can best be controlled by the judicious use of the ventilators.

WALTER M. MORGAN

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Acknowledgements T h e Glasshouse Crops Research Institute is funded through the Agricultural and Food Research Council. T h e work formed part of a commission by the Ministry of Agriculture, Fisheries and Food. I also wish to thank S. A. M o l y n e u x for her technical assistance, R. J. White and T . J. Dixon for advice on statistical analysis and D. M. Spencer and M. H. E b b e n for helpful discussions.

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