Introduction

Tomato (Solanum lycopersicum) is considered to be the second-most important vegetable crop after potato (Solanum tuberosum) worldwide, with an estimated yearly production of approximately 159 million tons from more than 4.8 million hectares of cropland (Faostat 2012). Tomato refers to a highly economically important crop in Japan, and the progresses in greenhouse cultivation over the past few years have made soil-borne diseases becoming one of the major constraints in the production of various economically important crops. Ralstonia solanacearum, one of the most devastating bacterial diseases (Genin and Denny 2012), accounts for severe tomato yield reductions in Japan. Soil fumigants (e.g., methyl bromide (MB)) have been the most frequently used approaches to control soil-borne diseases over the last few decades (McSorley et al. 2009; Zasada et al. 2010). However, they are being gradually abandoned for their contribution to stratospheric ozone depletion (Giannakou et al. 2002). For this reason, nonchemical soil disinfection methods are proposed to replace MB. Among these methods, soil solarization is considered to be one of the most promising methods to control soil-borne diseases (Katan 1981). Soil solarization involves heating the soil by covering it with polyethylene sheets (PE) and irrigating (Gill et al. 2009). Accordingly, the solar radiation can be retained in the warm season (July and August), and the high temperature and excessive moisture can eliminate soil-borne diseases (Horowitz et al. 1983; Abdallah 1991). Compared with pesticides, such method exerts a lower impact on the environment, humans, and animals (Gill and McSorley 2010, Gill et al. 2017; Gill 2014). The treatments of soil solarization involve either open field or greenhouse cropping systems, in the open field solarization seems to be less effective. The mentioned treatments have been successful only against Sclerotinia minor, Sclerotinia sclerotiorum, and Rhizoctonia solani in Sicily and in Tuscany (Triolo et al. 1985, 1989; Cartia 1987), also control of Verticillium wilt with soil solarization has been reported in warmer regions worldwide in the open field (Tjamos and Paplomatas 1988; Morgan et al. 1991; Ghini et al. 1992; Melero Vara et al. 1995). Furthermore, soil solarization has been popularized in greenhouse owners globally; only in Japan, the area has covered more than 5000 ha (Stapleton 2000).

Most studies on soil solarization focused on its disinfection effect, which has been demonstrated to adequately control cucumber vine wilt, pepper plague, pea blight, as well as root-knot nematodes of cucumber–tomato (Satour et al. 1991; Butler et al. 2014). Besides, numerous researchers tested PE mulch materials at different thicknesses and colors to enhance soil solarization efficiency (Cascone et al. 2012; Castello et al. 2017; D’Emilio 2017a). For soil temperature and exposure time, DeVay (1990) reported that 37 °C for two to four weeks is critical to pathogen control, while Stapleton and DeVay (1995) suggested that considerable harmful organisms in the soil are controlled by temperatures over 39–40 °C. According to Wang et al. (2004), a treatment of 2 min at 52 °C killed 100% of Cydia pomonella Linnaeus (Lepidoptera: Tortricidae) larvae, while Sonku and Nomura (1987) found that the density of R. solanacearum decreased markedly with the average daily soil temperature exceeded 40 °C for 10 consecutive days under soil solarization. It is generally known that soil solarization is the most effective when applied in the hottest months of the year and in areas with a warm climate (Horowitz et al. 1983; Mahrer et al. 1987; Stapleton 2000; Gill et al. 2009; D’Emilio 2017b). However, since meteorological conditions vary significantly with regions, the conditions associated with the optimal disinfection effect require in-depth exploration. Thus far, few researchers have employed quantitative methods to associate meteorological conditions with disinfection effects.

The present study aimed to investigate the relationships between the disinfection effect of soil solarization in the greenhouses and meteorological conditions in tomato cultivation by exploring the soil temperature, the population density of the pathogenic bacterium R. solanacearum before and after soil disinfection, the air temperature inside and outside the greenhouse, the amount of solar radiation, as well as rainfall.

Materials and methods

Overview of the survey field

The survey field used in the present study was in Kaizu City, which is located in the southernmost part of the Gifu Prefecture in Japan (35°13′ N, 136°38′ E). The region is situated between the Ibi River in the west and the Kiso-Nagara River in the east. Tomato cultivation began in this area in 1956, and the present acreage is approximately 30 ha. The production of winter–spring tomato is the primary crop in the Gifu Prefecture. Soil solarization started about 30 years ago, registered in the “Gifu clean agriculture” in 2003 (JA NiShiMiNo), and all tomato farmers have aimed to reduce pesticide use.

This study was carried out in five greenhouses in Kaizu City, named “A”, “B”, “C”, “D”, and “E”. The survey was conducted during the summer from 2010 to 2012 (July–September): the “A” and “B” greenhouses were surveyed in 2010–2012, while the “C”, “D”, and “E” greenhouses were surveyed only in 2012. As the time of planting and harvesting varies from farm to farm, there is a big difference in the disinfection period in each greenhouse. Among the five greenhouses in which the experiment was conducted, “A”, “B”, and “E” greenhouses were kept a closed state during the whole treatments, while in “C” and “D” greenhouses the farmers did not detect R. solanacearum in the previous year and thus the interest in soil solarization was low, resulting in the greenhouses not being suitably insulated during the entire disinfection period. Table 1 shows the dimensions, type, various characteristics of the covering material and disinfection period of the test fields. In Table 1, it is evident that the volume, structure, aspect, covering material, thickness and age of film of the five greenhouses vary greatly. The “B” greenhouse had the largest volume of 7246 m3, while the volume of the “A” greenhouse had the smallest at 3504 m3. The others ranged between 5279 and 5754 m3. Except for the “B” greenhouse, the thickness of the covering film for other greenhouses was 0.01 mm. All greenhouses updated film in 2012. Based on manufacturer, the solar transmittance and infrared ray barrier (IR barrier) of all greenhouses remained above 80%, and changed little with the year. The cultivated crops included the winter spring tomato varieties ‘Momotaro J’ and ‘Reiyou’, and the same varieties were planted in each greenhouse. The soil texture was mainly classified as loam (L) and silt loam (SiL). The soil physical conditions were similar in all the greenhouses. Soil particle and bulk densities increased toward the lower layer, soil particle density ranged from 2.56 to 2.68 g cm−3, and bulk density ranged between 1.00 and 1.57 g cm−3. Soil permeability decreased toward the lower layer, and all of the greenhouses were in rotational paddy fields. A low permeability layer was present at around 35 cm depth in all of the greenhouses, while the permeability was relatively high across the entire soil layer in the “B” greenhouse.

Table 1 The dimensions, type, various characteristics of the covering material and disinfection period of the test fields
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Survey items

In the approximate center of each greenhouse, the air temperature was measured at a height of 1.5 m from the field surface. Soil temperatures were measured using a thermometer (TR–72U, T&D Corp., Matsumoto, Japan) at depths of 15, 35, and 50 cm in each greenhouse. The measurement interval of the above items was 10 min. Moreover, the meteorological data in this region were obtained from the Automated Meteorological Data Acquisition System (AMEDAS) weather data (air temperature, precipitation, sunshine duration) of the neighboring Aisai City in the Aichi Prefecture. The amount of solar radiation can be estimated from the following Eq. (1) (Ministry of Agriculture, Forestry and Fisheries Agricultural Structure Improvement Bureau 1997):

$$S = \, Q_{\text{a}} \times \, \left( {0.18 + 0.55 \times N/N_{0} } \right)$$
(1)

where S denotes the daily amount of solar radiation (MJ m−2), Qa represents the daily amount of solar radiation outside the atmosphere (MJ m−2), N is the daily sunshine duration (h), and N0 is the daily possible duration of sunshine calculated from the latitude of the test site (h).

In this study, soil solarization was performed by first plowing the respective areas, and then covering them with polyethylene sheets; subsequently, sufficient irrigation was applied. The water requirements for saturation ranged from 78.9 to 174.0 mm, which were calculated based on the gas phase ratio of the target soil layer from the surface layer to the groundwater level. The aim of irrigating was to convert the soil into the reduced state by increasing the soil moisture; as a result, the thermal conductivity of the soil was enhanced, and the transfer of solar heat to the soil was facilitated. It is also useful to increase relative humidity during the day so creating an even more lethal environment for pests. After the soil was disinfected, the sheet was withdrawn, and tomatoes were planted after greenhouse ventilation for about 1 week.

Furthermore, in order to confirm the effect of soil disinfection, soil samples were collected at two points in each greenhouse, and the population density of R. solanacearum before and after disinfection was examined. About 10 g of soil sample was collected at the 15, 35, and 50 cm soil layers in each greenhouse, and R. solanacearum was detected using a culturing experiment with tetrazolium chloride medium (TZC), which is a type of selective medium (Kelman 1954; Liu et al. 2011). At each sampling point, the soil suspension was diluted by three stages of 10, 102, and 103 times with sterile water, and each stage used three plate medium, and then each plate medium was incubation at 28 °C by 72 h.

Results and Discussion

Solarization period and climatic conditions

Table 2 indicates the solarization period and climatic conditions (e.g., average daily air temperature, maximum air temperature, minimum air temperature, total solar radiation, average daily solar radiation, total precipitation, and precipitation days) in each greenhouse. The soil disinfection was performed nine times totally from July 28, 2010, to September 12, 2012, in the five greenhouses. The disinfection period in the “D” and “E” greenhouses was the shortest at 19 d and 18 d in 2012, respectively, while the “A” greenhouse was the longest at 33 d in 2010. The average soil disinfection period was 24 d. The average daily solar radiation was the lowest at 16.7 MJ m−2 in the “C” greenhouse and the highest in the “D” greenhouse at 22.1 MJ m−2. The average value of all greenhouses was 18.7 MJ m−2. The average daily maximum and minimum air temperature values outside the greenhouse were almost higher than 36 °C and 21 °C, respectively, and the temperature difference between the two was approximately 15 °C. The average daily air temperature outside the greenhouse during the disinfection period was 28.2 °C, with the lowest value of 27.2 °C detected outside the “C” greenhouse in 2012, while the others ranged from 27.9 to 28.8 °C. Inside the greenhouses the air temperature differed from each other, with the maximum temperature of 40.9 °C recorded in the “A” greenhouse in 2012 and the minimum temperature of 32.4 °C recorded in the “C” greenhouse in 2012. The average daily temperature was 36.9 °C. Precipitation occurred during the entire disinfection period, with the lowest value of only 16 mm in the “D” greenhouse with two precipitation days, followed by the “E” greenhouse with 32 mm in 3 d; meantime, the total precipitation and precipitation days of the other greenhouses ranged from 34 to 170.5 mm and 6–9 d, respectively.

Table 2 Solarization period and climatic conditions inside and outside the greenhouses
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Soil temperature and disinfection effect

According to previous soil solarization studies, R. solanacearum is killed under average daily soil temperatures exceeding 40 °C for 10 consecutive days (Sonku and Nomura 1987). Accordingly, the standard temperature was set to 40 °C.

Table 3 presents the total days and the maximum consecutive days that the average daily soil temperature reached the standard temperature, soil temperature as well as the population density of R. solanacearum before and after soil solarization. The unit represents the number of colony-forming units (cfu) in 1 g of dry soil. The shaded parts show the days that fulfilled the sterilization conditions for R. solanacearum. The “A” greenhouse from 2010 to 2012 and “B” greenhouse in 2010 met the sterilization conditions for R. solanacearum only to the depth of the 15 cm layer. Conversely, the “B” greenhouse in 2011 met this criterion until the 50 cm soil layer. The “D” and “E” greenhouses reached the standard temperature at 15 cm, but not for 10 consecutive days. The “C” greenhouse did not reach the standard temperature in any of the layers.

Table 3 The total days and maximum consecutive days of the daily average soil temperature reaching the standard temperature (40 °C), soil temperature and the population density of R. solanacearum
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The boxed sections in Table 3 indicate a superior disinfection effect, as R. solanacearum was not detected after soil solarization. In the “A” greenhouse, R. solanacearum was detected at 15 cm depth in 2011 and 2012 before solarization, whereas it was not detected after soil solarization. In the B greenhouse, R. solanacearum was detected at 15 cm depth in 2010 and at 15 cm and 35 cm depth in 2011 before solarization, whereas it was not detected in all layers after solarization. In the “B”, “C”, “D”, and “E” greenhouses in 2012, R. solanacearum was detected both before and after solarization, which indicated that the disinfection effect was small. On the contrary, a phenomenon whereby the number of bacteria increased and the distribution area shifted to a deeper layer was observed in the “C” and “D” greenhouses. A detailed analysis of this result would have required a greater number of sampling points and a statistical analysis. However, the finding that the treatments were ineffective is adequate for the purposes of this work. As revealed from a comparison of the soil temperature and disinfection effects, the results of Table 3 were consistent with each other. When the average daily soil temperature exceeded 40 °C for more than 10 consecutive days, soil solarization exerted a good disinfection effect on R. solanacearum, as observed in the “A” and “B” greenhouses over three years, except for the “B” greenhouse in 2012. On the contrary, the disinfection effect of the “C”, “D”, and “E” greenhouses was poor, as they did not meet the above-mentioned disinfection conditions for R. solanacearum.

Meteorological conditions analysis

Meteorological conditions of the entire disinfection period

Soil temperatures are directly related to meteorological conditions, so the meteorological conditions are considered as an important factor that greatly influences the soil solarization efficiency. It was confirmed that the disinfection effect was poor in the “B”, “C”, “D”, and “E” greenhouses in 2012 (Table 3). In comparison with the greenhouses with good disinfection effects, the “B” greenhouse in 2012 had moderate average daily solar radiation and average daily air temperature values, and thus the standard temperature at the 15 cm layer was reached a total of 12 d, covering 4 d (8/7–8/10) and 8 d (8/17–8/24) (Fig. 1). However, between the above two periods (8/11–8/16), there were three rainy days. The total rainfall was 46.5 mm and the average daily solar radiation was remarkably low (14.1 MJ m−2) during these 3 days; as a result, the impact of the rainy and cloudy days was considered as the main contributor to the poor disinfection effect (Fig. 1). However, as the standard temperature was met on 8 and 4 d, a certain disinfection effect was exerted though R. solanacearum was still detected after solarization. As shown in Fig. 1, if there were some rainy days during soil solarization, the solar radiation or air temperature dropped, the period where the average daily soil temperature exceeded 40 °C was cut off, and the condition for 10 consecutive days could not be achieved. Then, good disinfection effect could not be realized. In the “C” greenhouse, the disinfection period was relatively late (8/23–9/12), resulting in the average daily solar radiation (16.7 MJ m−2), the average daily air temperature (27.2 °C), and the minimum and maximum average daily air temperature (20.3 °C and 34.6 °C) being the lowest of all the greenhouses (Table 2). Moreover, although the total precipitation was low, there were more cloudy and precipitation days (Fig. 2). In addition, the greenhouse was not suitably insulated throughout the disinfection period. Finally, the average daily soil temperatures in the 15 cm, 35 cm, and 50 cm layers in “C” were 35.4 °C, 34.2 °C, and 33.6 °C, thereby not exceeding 40 °C in all soil layers. In the “D” and “E” greenhouses, the disinfection period experienced better meteorological conditions compared with the other greenhouses, and thus a better disinfection effect should have been achieved. However, of all the soil layers studied, only the average daily soil temperature in the 15 cm layers exceeded 40 °C. Furthermore, the maximum consecutive days were only 1 d (“D” greenhouse) and 2 d (“E” greenhouse) (Table 3). The main reason why the “D” and “E” greenhouses did not reach 40 °C or higher for more than 10 d was that the disinfection period was too short (“D”:19 days, “E”:18 days). It is well known that increases in soil temperature require time. For example, in the “E” greenhouse (Fig. 3), although the solar radiation and air temperature were better in the first two days of disinfection, it was followed by rain and cloudy days (4 d). It thus took several days for the soil to return to its original temperature before the rain; the disinfection effect was small. In addition, the “D” greenhouse also had the problem of poor insulation, which also made the soil temperature not meet the standard temperature for more than 10 days. The common issue with the “B”, “C”, “D”, and “E” greenhouses in 2012 was that the disinfection period was short. Therefore, in terms of the entire disinfection period, the greenhouse with good disinfection effect satisfied the following conditions: the disinfection period exceeded 24 d, the average daily solar radiation was above 17.0 MJ m−2, and the average daily air temperature was above 28.0 °C.

Fig. 1
figure 1

The effect of rainy and cloudy days on the soil temperature of the 15 cm layer in the “B” greenhouse in 2012

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Fig. 2
figure 2

The meteorological conditions and average daily soil temperature of the 15 cm layer in the “C” greenhouse in 2012

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Fig. 3
figure 3

The meteorological conditions and average daily soil temperature of 15 cm layer during soil solarization in the “E” greenhouse in 2012

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Another important climatic factor affecting the soil temperature refers to the air temperature inside the greenhouse. The air temperature inside the greenhouse can be complicatedly affected by the airtightness of the greenhouse, the number of days closed, the average air temperature during treatment period, etc. Under the same air temperature outside the greenhouses in 2012, the air temperature inside the “A” greenhouse was the highest, while that inside the “C” and “D” greenhouses was the lowest. As mentioned above, the two greenhouses were poorly insulated, revealing that the airtightness of the greenhouse during the soil solarization is important.

Meteorological conditions of meeting the standard condition

Table 4 indicates that the climatic conditions of the greenhouses met the standard temperature of higher than 40 °C for longer than 10 consecutive days in each soil layer under soil solarization.

Table 4 Climatic conditions of the greenhouses that met the standard temperature (40 °C) for more than 10 consecutive days in each layer by soil solarization
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For the “A” greenhouse, from 2010 to 2012, the criterion of 10 consecutive days exceeding 40 °C was only met in the 15 cm layer, and the days that the average soil temperature met this criterion were 11 d (2010), 10 d (2011), and 13 d (2012).

For the “B” greenhouse, an average soil temperature exceeding 40 °C for 10 consecutive days was observed in 2010 and 2011. In 2010, the average soil temperature met the standard condition only in the 15 cm layers with the period of 13 d. In contrast, in 2011, the conditions were met in all layers, with the period of 17 d, 14 d, and 11 d, respectively. From the perspective of the entire disinfection period, the average solar radiation, the average daily air temperature inside and outside the greenhouse by the “B” greenhouse in 2011 were the worst among all good disinfection effect greenhouses (Table 2); however, it had achieved the best soil disinfection effect up to the depth of 50 cm. The disinfection period in the “B” greenhouse in 2011 was from July 28 to August 24 (28 d). At the end of the disinfection period (8/15–8/24, excluding 8/18), it was rainy and cloudy with 145.5 mm rainfall, and the rainfall during the entire period was primarily concentrated in the above period. The disinfection period of the “A” greenhouse and the “B” greenhouse in 2011 was almost the same, except that the “A” greenhouse was delayed by 4 d (Fig. 4). However, the “B” greenhouse obtained a good disinfection effect in all soil layers. One explanation is the cumulative effect of temperature on the sunny days. Before the average daily soil temperature first reached 40 °C in the 15 cm layer in the “B” greenhouse, six out of the 7 days were sunny. In addition to the rainy days mentioned above (8/15–8/24), the other days were sunny except for three rainy and cloudy days, in which the average daily solar radiation reached 20.7 MJ m−2, thereby a higher soil temperature was achieved. The maximum average daily soil temperature in the 15 cm layer reached 47.5 °C, and there were 8 days when an average daily soil temperature higher than 45 °C was achieved; as a result, there were even four rainy and cloudy days among 8/15–8/20, the average daily soil temperature in these days also reached over 40 °C (Fig. 4). Moreover, the correlation between the soil temperature in 15 cm layer and other soil layers (35 and 50 cm) was very high, which was achieved by high heat transmission of saturated soil. It is therefore indicated that a better disinfection effect was obtained from the surface layer to the 50 cm soil layer in the “B” greenhouse in 2011.

Fig. 4
figure 4

The meteorological conditions and average daily soil temperature of 15 cm layer during soil solarization in the “A” and “B” greenhouse in 2011

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In this survey, the meteorological conditions necessary for the elimination of R. solanacearum via soil solarization were analyzed. When the standard temperature of higher than 40 °C for more than 10 consecutive days was reached in the 15 cm layers, the average daily solar radiation was 20.2 MJ m−2, the average daily air temperature inside and outside the greenhouse was 41.0 °C and 29.3 °C, respectively (Table 4). For the 35 cm and 50 cm layers, only the B greenhouse met the above condition in 2011, with an average daily solar radiation of about 18.2 MJ m−2, as well as an average daily air temperature inside and outside of about 39.0 °C and 29.1 °C, respectively (Table 4).

However, if the disinfection period was late (e.g., in the “C” greenhouse), then the air temperature and solar radiation were low, and thus the soil temperature did not rise rapidly enough. In this scenario, it is better to perform soil solarization during the high temperature period. When the disinfection period was short, for example in the “D” and “E” greenhouses (19 and 18 d), additional time was required for the soil temperature to rise. Furthermore, rainy and cloudy days sometimes lowered the soil temperature. Even if the soil temperature rose, there was insufficient time for the necessary conditions to be met. The disinfection period should thus last more than 24 d. While the meteorological conditions during the disinfection period were good in the “D” greenhouse, good disinfection results were not achieved. This was mainly due to the fact that the lower temperature inside the greenhouse influenced the increase in soil temperature, and it is thus necessary to ensure that greenhouses are insulated during the soil disinfection period (Dai et al. 2016). Likewise, in the “C” greenhouse, the bad insulation made the soil temperature significantly differ from other greenhouses. In addition, even under the better meteorological conditions, the disinfection effect was also affected by the characteristics of covering, the state of aging, and the volume of the greenhouse, etc. However, in this study, in 2012, the all the covering materials were updated, and the solar transmittance and IR barrier were the same conditions in all greenhouses, so the results of this year should not consider the effects of the characteristic of covering materials. Furthermore, comparing the 3 years of “B” greenhouse, it should have a lower disinfection effect of the aging of the covering material in 2010 and 2011 than 2012, whereas a sufficient effect was achieved, so it could be determined that the low effect in 2012 resulted from meteorological conditions. Hence the conclusion in this study was limited to the conditions in Table 1.

Conclusions and Recommendations

In a survey of soil solarization in five greenhouses from 2010 to 2012, it was found that the disinfection effect of soil solarization and the meteorological conditions during the disinfection period are closely associated. For the entire disinfection period, the greenhouses with good disinfection effects satisfied the following conditions: the disinfection period exceeded 24 days, the average daily solar radiation was above 17.0 MJ m−2, and the average daily air temperature was above 28.0 °C. For the 15 cm soil layer of all the greenhouses to meet the necessary conditions of average daily soil temperature exceeding 40 °C for more than 10 consecutive days, the average daily solar radiation exceeded 20.2 MJ m−2, and the average daily air temperature inside and outside the greenhouse exceeded 41.0 °C and 29.3 °C. These parameters can be affected by other factors such as the insulation of the greenhouse, rainy and cloudy days, the characteristics of covering, the state of aging, solar transmittance, IR barrier, etc. In addition, when the meteorological conditions are poor, organic substances (e.g., molasses) can be applied to the soil during solarization and can shorten the disinfection days (Shinmura 2003) and also achieve better disinfection effects. Further investigations are required to evaluate the relationship between disinfection effect and the necessary meteorological conditions when using this anaerobic soil disinfection method.