Comparison of Epidemiology of Gray Mold, Anthracnose Fruit Rot, and Powdery Mildew in Day-Neutral Strawberries in Field and High-Tunnel Conditions in Ontario

Abstract

Anthracnose fruit rot (Colletotrichum acutatum), Botrytis gray mold (Botrytis cinerea), and powdery mildew (Podosphaera aphanis) are major fruit diseases affecting strawberries in Ontario, but the epidemiology and management of these diseases in day-neutral strawberries in high-tunnels plantings are not well understood. Incidences of both Botrytis gray mold (BGM) and anthracnose fruit rot (AFR) were very low in tunnel plots, compared to outdoor plots (5-fold lower BGM incidence and 5–20-fold lower AFR incidence); whereas the incidence of powdery mildew (PM) on berries was higher in the tunnel plots compared to outdoor field plots. BGM incidence was observed in the first two harvest weeks and decreased thereafter in the outdoor plots, where as incidence of BGM was negligible in the tunnel plots. The AFR was first observed in the first week of August and the last week of July in 2009 and 2010, respectively, The epidemics of PM increased after the second week of September in both years. In outdoor field plots, Maestro 80 DF and Nova 40 W or Pristine WG provided good control of BGM and AFR. ‘Seascape’ had significantly lower AFR than ‘Albion’; whereas PM incidence was higher in ‘Seascape’. There were significantly higher (P < 0.01) cumulative marketable fruit numbers (1- to 3-fold higher) and marketable fruit yields (2- to 3.5-fold higher) in tunnel plots than outdoor plots in both years.

Keywords:

• Fragaria x ananassa
• fungal disease
• protected culture

INTRODUCTION

The cultivation of day-neutral strawberries is increasing in Ontario in order to provide fresh strawberries for 4–5 months. Historically, June-bearing strawberries, whose production season lasts 5–6 weeks in Ontario, have been widely cultivated, and off-season supplies of strawberries were dependent on imports. Breeding programs have been diverted towards developing Ontario adapted day-neutral cultivars and research is focusing on the evaluation of existing day-neutral cultivars, and improving cultivation practices, including high-tunnel production and epidemiological studies for diseases and pests.

Anthracnose fruit rot (AFR) caused by Colletotrichum acutatum, Botrytis gray mold (BGM) caused by Botrytis cinerea, and powdery mildew (PM) caused by Podosphaera aphanis are major fruit diseases of strawberry in Ontario and other strawberry growing areas of the world (Carisse and Bouchard, 2010; Dale et al., 2000; Smith, 2008; Xu et al., 2000). AFR and BGM cause fruit rots and reduce yield and marketability. Colletotrichum spp. also can infect the crown, leaves, stolons, and petioles of the strawberry. Podosphaera aphanis infects both foliar and floral parts of strawberries. It can cause mildew on leaves, flowers, buds, and fruit. Fruits will be small, deformed, and covered with white mildew, reducing the fruit yield and marketability (Mass, 1998). Latent infection of floral parts is the avenue and source of BGM development on fruit and the disease spread is influenced by pre-harvest temperature and period of wetness or moisture-related variables, relative humidity, and rainfall (Bristow et al., 1986; Bulger et al., 1987; Wilcox and Seem, 1994). Wilson et al. (1990) found that temperatures between 15–25°C and longer leaf wetness duration are favorable for AFR. Podosphaera aphanis does not need free moisture to infect the strawberry and high humidity and temperature will favor the disease epidemics (Blanco et al., 2004; Miller et al., 2003).

Day-neutral strawberry cultivars require different cultivation approaches than June-bearing strawberry cultivars. Due to the longer production period and later ripening period of day-neutral strawberries, insect and disease management practices will differ from the traditional June-bearing production system. The epidemics and management of fruit and foliar diseases in day-neutral strawberries are not yet well understood under Ontario conditions. The objectives of this study were: (i) to compare the epidemiology of AFR, BGM, and PM on 2 day-neutral strawberry cultivars under field and high-tunnel conditions; and (ii) to evaluate captan (Maestro 80 DF), boscalid+pyraclostrobin (Pristine WG), and mycobutanol (Nova 40 W) in the control of these diseases.

MATERIALS AND METHODS

The experiments were conducted at the University of Guelph's Cedar Springs Research Station, located in southwestern Ontario during the 2009 and 2010 summer and fall seasons. This site contains a Fox Gravelly Loam soil (47.8% sand; 38.1% silt; 14.1% clay) and receives between 3,300 and 3,500 Corn Heat Units per year. Plots were established outdoors and under Haygrove high-tunnels (8.5 m wide, 4.25 m high, 45 m long). Dormant strawberry crowns were established on raised beds covered with 1.0 mm black plastic mulch, under which a single drip irrigation tape was installed. Crowns were planted in double staggered rows with 20.0 cm in-row spacing and 30.0 cm row width in early May of each year. Irrigation was scheduled using tensiometers, and fertilizer (Plant Products 20-20-20) was applied weekly through the irrigation, for a season total nitrogen application of 80 kg/ha. Flowers were removed from the plants for 4 weeks after planting to promote the vegetative growth. Runners were regularly cut to promote fruit production throughout the season.

Weather stations were installed and equipped with temperature, relative humidity, leaf wetness, wind speed, and rainfall sensors. One weather station was located inside the plastic tunnel and the other was installed near the outdoor plots. Hourly weather data: temperature, leaf wetness duration, rainfall, and wind speed were collected throughout the crop season.

Two day-neutral cultivars developed in California, Seascape and Albion, were evaluated to compare susceptibility to BGM, AFR, and PM under outdoor field and in high-tunnels. Incidences of these three diseases were compared when using a 7-day interval captan-spray (Maestro 80 DF) versus non-sprayed (control) plots. The 2010 trial included an additional treatment of Pristine WG or Nova 40W applied alternatively at 10-day intervals. The spray rates of Maestro 80 DF, Pristine WG, and Nova 40W were 4.5 kg/ha, 1.3 kg/ha, and 340 gm/ha, respectively. The plots were arranged in factorial randomized complete block design with four replicates for each treatment. Fungicides were applied using a backpack pressurized small plot sprayer. Fruit was harvested twice a week from the last week of July to the last week of October. The total number of fruit and fruit infected with BGM, AFR, and PM were counted. Harvested fruit were categorized as marketable or unmarketable, and yields were recorded at each harvesting. Mean and standard error of cumulative percent incidence of BGM, AFR, and PM were calculated for fungicide sprayed and non-sprayed plots in both outdoor and high-tunnel plot experiments. Weekly incidences of these three diseases were also compared and relationships of disease incidence with weather variables were also analyzed. Analysis of variance (ANOVA) was performed using SAS V9.1 (SAS Institute Inc., Cary, NC, USA) to compare the cumulative incidence of these three diseases and marketable fruit yields between fungicide-sprayed and non-sprayed plots and between outdoor and high-tunnel experiments.

RESULTS AND DISCUSSION

Incidences of Botrytis Gray Mold (BGM) and Anthracnose Fruit Rot (AFR)

The incidence of three fruits diseases were recorded from the last week of July to the last week of October in both years. BGM incidence was very low in both 2009 and 2010 in outdoor fields as well as in the tunnel. However, BGM incidence was relatively higher in 2010 field plots compared to 2009. In 2010, the BGM incidence was 10–15% of all fruit harvested from the last week of July to the first week of August; the disease incidence was <5% thereafter in outdoor plots. BGM incidence was 5-fold lower under tunnel plots compared to outdoor fields (Table 1).

TABLE 1 Comparison of Cumulative Incidences of Botrytis Fruit Rot (BFR), Anthracnose Fruit Rot (AFR), and Powdery Mildew (PM), and Marketable Berry Yields of Unsprayed Plots in Outdoors and in High Tunnels

Parameter ^z	Year	Cultivar	Outdoor plots	Tunnel plots
IBFR	2009	Seascape	Negligible	Negligible
		Albion	Negligible	Negligible
	2010	Seascape	1.57	0.31
		Albion	1.65	0.39
IAFR	2009	Seascape	22.89	5.27
		Albion	32.93	4.53
	2010	Seascape	10.68	0.7
		Albion	20.30	0.9
IPMIF	2009	Seascape	4.89	11.52
		Albion	5.11	12.89
	2010	Seascape	3.83	13.95
		Albion	0.62	6.95
CMFN	2009	Seascape	141	185
		Albion	110	189
	2010	Seascape	105	160
		Albion	69	229
CMFW (gm)	2009	Seascape	1,170	2,417
		Albion	1,109	2,450
	2010	Seascape	835	1,466
		Albion	793	2,816
^zIBFR = incidence of Botrytis fruit rot, IAFR = incidence of Anthracnose fruit rot, IPMIF = incidence of powdery mildew infected fruits. Incidence of all three fruit diseases were calculated as percent cumulative incidence. CMFN = Cumulative marketable fruit number, CMFW = cumulative marketable fruit weight per plot (1.2 m^2). Harvesting was started on July 30th and 19th in 2009 and 2010, respectively, and ended in the last week of October in both years.

The weekly average AFR infection from the non-sprayed plots was compared between outdoor plots and high-tunnel plots (Figs. 1A and 1B). AFR was first observed in the first week of August and the last week of July in 2009 and 2010, respectively (Figs. 1A and 1B). The AFR incidence in the tunnel plots was significantly lower (P < 0.01) than in outdoor field plots in both years. In the fungicide non-sprayed plot, the cumulative AFR incidence was 5- to 22-fold lower in the tunnel plots compared to outdoor plots (Table 1, Fig. 2A). The infection periods of AFR were variable between the two years in outdoor plots. The AFR incidence was relatively higher in the cultivar Albion when compared to Seascape; however, the resistance levels of these two cultivars were variable between the two years (Figs. 1A and 1B). In 2009, the AFR incidence was low (<15%) until the third week of August and increased thereafter until the last week of September (Fig. 1A). In contrast, the AFR incidence was higher in the initial three harvesting weeks (19 July to 2 August), but decreased thereafter until the last week of August in 2010 (Fig. 1B). The disease incidence was relatively lower in September in 2010 than 2009 (Figs. 1A and 1B). There was a greater difference in the AFR incidence between the two cultivars in 2010 than in 2009.

FIGURE 2 Cumulative disease incidence and marketable fruit yields of ‘Albion’ and ‘Seascape’ strawberry in Captan-sprayed plots and unsprayed plots in outdoor and high-tunnel environments. (A) Anthracnose fruit rot; (B) Powdery mildew; (C) Marketable fruit numbers; (D) Marketable fruit yields (gm).

FIGURE 1 Average weekly incidences of Anthracnose fruit rot and powdery mildew in unsprayed ‘Albion’ and ‘Seascape’ day-neutral strawberries in an outdoor field and tunnel plots in 2009 and 2010. (A) and (B) Anthracnose fruit rot; (C) and (D) Powdery mildew on fruit.

The AFR epidemics in outdoor plots were highly dependent on weather variables. The moisture-related weather variables (amount, period, and frequency of rainfall; relative humidity; and leaf wetness period) and temperature influenced disease occurrence (Fig. 3). In 2009, the frequency and amount of rainfall was lower during the last week of July to the second week of August and resulted in reduced disease incidence. In 2010, a hot and dry period during the first to third weeks of August resulted in low AFR incidence. Longer periods of free moisture or wetness are required for conidial germination and optimum temperature (15–25°C) favors the infection and latent period (Wilson et al., 1990; Smith, 2008). Rain splash is the principal means for conidia dispersal of Colletotrichum from infected to healthy plants (Madden and Wilson, 1997). Rainfall and temperature was highly associated with AFR incidence in both years (Fig. 3).

FIGURE 3 Weather variables recorded in outdoor and high-tunnel environments. (A) Daily rainfall in 2009 and 2010; (B) Daily average temperature and relative humidity (RH) in 2009; (C) Daily average temperature and RH in 2010 (color figure available online).

Very low incidences of BGM and AFR in the high-tunnel plots in both years suggest that there was no need to spray fungicides to control BGM and AFR under the high-tunnel in this experiment (Table 1, Figs. 1 and 2). High-tunnels prevent the rainfall on the plots and, therefore, disease dispersal from infected to healthy plants via rain splashing will be reduced. Temperature was relatively higher and relative humidity was lower in tunnel plots compared to outdoor plots (Figs. 3A and 3B), which could also reduce disease incidence under high-tunnel plots. Xiao et al. (2001) found lower BGM incidence in tunnel plots compared to outdoor fields. They reported that higher temperature and shorter duration of wetness reduces gray mold incidence.

Incidence of Powdery Mildew on Strawberry Fruits

Powdery mildew on fruit was observed in the last week of August and increased after the second week of September until harvest was completed in both years (Figs. 1C and 1D). The cultivar Seascape had a higher disease incidence than the cultivar Albion. The disease incidence was significantly higher (P < 0.01) in tunnel plots compared to outdoor plots. Once the disease appeared in the field, it gradually increased during the last few weeks of harvest. PM symptoms were also observed on leaves, buds, flowers, and young fruits in both years. Lower relative humidity, relatively dry and warm temperatures, and low light intensity under high-tunnel plots may contribute to increased powdery mildew. The results were consistent with Xiao et al. (2001), who also reported higher incidence of powdery mildew in tunnels than outdoor plots.

Effect of Fungicides on Fruit Rots and Yield

Captan sprays at 7-day intervals and alternate sprays of Nova 40W and Pristine WG at 10-day intervals significantly reduced both AFR and BGM and also increased marketable fruit numbers and yields (Fig. 2). In outdoor plots, the cumulative incidence of AFR was lower in Captan-sprayed plots compared to control plots, however, no difference was observed in AFR incidence in Captan-sprayed and control plots under tunnels (Fig. 2A). This suggests that there was no need to spray fungicide to control BGM or AFR rot in strawberries grown under high-tunnels. Captan sprays at 7-day intervals in 2009 and alternate sprays of Nova 40W and Pristine WG at 10-days intervals in 2010 did not reduce PM incidence significantly (Fig. 2B). New combinations of fungicides should be evaluated under high-tunnels to control the powdery mildew.

The number of marketable fruit and yields were higher in Captan-sprayed plots compared to control plots in both years in outdoor fields; however, no difference was observed between Captan-sprayed and control plots in the tunnel (Figs. 2C and 2D). Marketable fruit numbers and yields were consistently higher in tunnel plots than outdoor plots in both years, which suggest that growing day-neutral strawberries under tunnels provides better control of fruit rots and, thus, can increase the fruit yield. In addition, strawberries growing in high-tunnels are prevented from rain damage and cold stress, which also contribute to increased fruit yield.

CONCLUSION

Incidences of both BGM and AFR were very low under tunnel plots, compared to outdoor plots. Marketable fruit numbers were 1.5- to 3-fold higher and marketable fruit yields were 2- to 3.5-fold higher in the tunnel plots compared to outdoor fields. There was no need to spray fungicides under the tunnel plots to control BGM and AFR. ‘Seascape’ had better resistance to AFR than ‘Albion’, while ‘Albion’ had better resistance to powdery mildew and better yields in a tunnel environment. Captan applications at 7-day intervals and alternate applications of Nova 40W and Pristine WG at 10-day intervals provided better control of BGM and AFR in outdoor plots. The incidence of powdery mildew was higher in tunnel plots than outdoor plots. The effect of these fungicides on PM incidence was variable and needs further investigation for better control.

ACKNOWLEDGMENT

We thank the Ontario Ministry of Agriculture, Food, and Rural Affairs (OMAFRA) New Directions & Alternative Renewable Fuels Research Program for funding support (Project No. SR9222). We also thank Pam Fisher, OMAFRA Berry Specialist, for her valuable suggestions on the research project and Greg Watt, University of Guelph, for his technical help managing research trials.