Mauromicale et al.: Solarization for controlling of Orobanche ramosa • 877

Weed Science, 53:877–883. 2005

Soil solarization, a nonchemical method to controlbranched broomrape (Orobanche ramosa) and improvethe yield of greenhouse tomato

Giovanni MauromicaleCorresponding author. Dipartimento di ScienzeAgronomiche, Agrochimiche e delle ProduzioniAnimali—Universita degli Studi di Catania, ViaValdisavoia 5, 95123 Catania, Italy;g.mauromicale@unict.it

Antonino Lo MonacoAngela M. G. LongoAlessia RestucciaDipartimento di Scienze Agronomiche,Agrochimiche e delle Produzioni Animali—Universita degli Studi di Catania, Via Valdisavoia 5,95123 Catania, Italy

Tomato cultivation in the Mediterranean region is susceptible to infestation by theparasitic weed branched broomrape (Orobanche ramosa), and severe yield losses canresult. The effectiveness of solarization, a soil disinfection technique that uses passivesolar heating, to control the incidence of broomrape under greenhouse conditionswas studied over two growing seasons. Solarization was accomplished by the appli-cation of clear polyethylene sheets to moist soil for 58 to 61 d during the hot season.The treatment increased maximum soil temperature by around 10 C, and at 5 cmbelow the soil surface, a temperature of more than 45 C was reached for 34 to 58d, whereas this temperature was not reached at all in the first season and not for 20d (second season) in unmulched soil. In solarized soil, no broomrape shoots emerged,and neither haustoria nor underground tubercles of the parasite were found ontomato roots. The treatment killed about 95% of buried viable seed, and inducedsecondary dormancy in the remaining 5%. In nonsolarized plots, broomrape shootswere present at a high density, decreasing plant growth and fruit production. Fruityield was 133 to 258% higher in the solarized as compared with the nonsolarizedtreatment. Based on these results, we suggest that soil solarization, which precludeschemical contamination and is suitable for organic farming, is an appropriate tech-nology where the risk of branched broomrape infestation is high.

Nomenclature: Branched broomrape, Orobanche ramosa L. ORARA; tomato, Ly-copersicon esculentum Mill. ‘Ikram’.

Key words: Greenhouse production, tomato yield, soil solarization, soil tempera-ture, seed viability.

Parasitic weeds of Orobanche spp. cause serious damageto several crops in Europe, the Mediterranean region, Cen-tral Asia, the Arabian Peninsula and some African countries(Klein and Kroschel 2002). Most of the parasite’s life cycleoccurs belowground connected to the host plant and is,therefore, very difficult to control by either agronomic prac-tices or herbicides (Goldwasser et al. 2003). In addition,control is made difficult by the fact that each plant producesthousands of dust-like seeds of 0.2- to 0.3-mm-diam thatare readily distributed and remain viable in the soil for manyyears (Goldwasser et al. 2001). Although a broad spectrumof control methods has been attempted (cultural, physical,chemical, and biological), no significant reduction of infes-tation has been achieved. Hence, other control methods areneeded (Klein and Kroschel 2002).

Among the Orobanche species, branched broomrape (Oro-banche ramosa L.) is one of the most prevalent and devas-tating. Together with Egyptian broomrape (Orobanche ae-gyptiaca Pers.), it infests about 2.6 million ha of solanaceouscrops (primarily tobacco, potato, tomato, and eggplant),mainly in the Mediterranean basin, North Africa, and Asia(Boari et al. 2003; Qasem 1998; Zehhar et al. 2002). Incertain parts of Greece, Israel, Lebanon, and Jordan,branched broomrape has frequently damaged tomato, to-bacco, and potato fields, with 100% yield losses having beenrecorded (Goldwasser et al. 2001; Haidar et al. 2003; Lolas1994; Qasem 1998). Other crops in the Mediterranean re-gion commonly parasitized and severely impacted by

branched broomrape include sunflower, oilseed rape, andcarrot. It has become a recognized agronomic threat in west-ern France (Gibot-Leclerc et al. 2004) and has been record-ed for the first time in Australia, Central America, and theUnited States (Boari et al. 2003). In Italy, branched broom-rape is responsible for significant yield losses in tobacco,cabbage, and tomato (Boari and Vurro 2004; Boari et al.2003; Diana and Castelli 1994; Zonno et al. 2000) and hascaused damage to both field and greenhouse tomato cropsin southern Italy.

Tomato is the main field and greenhouse vegetable cropof the coastal areas of the Mediterranean basin (Tognoni andSerra 2003). In Italy, field cultivation occupies an area of133,000 ha and produces about 7,000 Mkg of fruit, whereasgreenhouse production occurs on about 7,500 ha. Pathogen,insect, and weed management in the greenhouse relies onregular preplant soil fumigation with methyl bromide,which also controls branched broomrape. However, the useof this fumigant is compromised by its destructive effect onatmospheric ozone (Noling and Becker 1994). As a result,its use is scheduled to be phased out between 2005 and2015, according to the revised Montreal Protocol. In theEuropean Union, use of methyl bromide as a soil, com-modity, and structural fumigant has been banned since Jan-uary 1, 2005 (European Regulation CE 2937/2000). There-fore, there is an urgent need to identify alternative technol-ogies for broomrape control. In southern Italy and otherMediterranean countries, an attractive alternative is soil so-

878 • Weed Science 53, November–December 2005

larization (Katan 1987; Mauromicale et al. 2001, 2005; Sta-pleton and DeVay 1986), alone or in combination with oth-er methods. This approach has attracted interest in manywarm-climate countries because of its effectiveness, simplic-ity, low cost, and safety for humans, animals, plants, andthe environment (DeVay and Katan 1991; DeVay and Sta-pleton 1997). Solarization entails covering wet soil withtransparent polyethylene sheets during the hot season (Katanet al. 1976). This serves to trap solar energy, thereby, heatingthe soil sufficiently to destroy soil pests and microbes. Thetemperature increase achieved is primarily the result of theelimination of evaporation, but is also partially because ofthe greenhouse effect created (Mahrer 1979). Its effective-ness has been demonstrated in many countries around theworld (Katan 1991). Soil solarization has proven to beamong the most effective methods of broomrape control inopen field crops (Haidar and Sidahmad 2000; Jacobsohn etal. 1980; Mauromicale et al. 2001; Sauerborn et al. 1989).

The main objective of this research was to evaluate theeffectiveness of soil solarization both for the control ofbranched broomrape in heavily and naturally infested green-house soils in southern Italy and for the improvement ofplant growth and fruit yield in the tomato crop. The effectof soil solarization on germination and viability of buriedbranched broomrape seeds was also examined.

Materials and Methods

Site, Climate and Soil

Greenhouse experiments were conducted during the 2002to 2003 and 2003 to 2004 seasons on the coastal plainsouth of Siracusa (Sicily), South Italy (lat 378039N, long158189E, 10 m above sea level [asl]) in a moderately deepCalcixerollic Xerochrepts soil naturally infested withbranched broomrape. Before solarization, the soil character-istics were 15.5% clay, 29.1% silt, 55.4% sand, and 2.0%organic matter with pH 7.6, 1.8‰ total nitrogen (N), 100ppm available phosphorus (P), and 680 ppm exchangeablepotassium (K). The local climate is semiarid/Mediterraneanwith mild winters and hot, rainless summers. The mean 30-yr maximum summer monthly temperatures are 29.6 C(June), 32.5 C (July), 31.6 C (August), and 27.3 C (Sep-tember).

Experimental Design and Soil Solarization

In both seasons, the experiments included two treatments,solarized and nonsolarized, arranged in a randomized designwith four replications. The plot size was 3 by 15 m in bothseasons. During late spring, the soil was ploughed severaltimes to provide a uniform surface and then leveled. Oneday before mulching, the soil was irrigated to field capacitybecause solarization is more effective with moist soil (Katan1981) because of the increased thermal sensitivity of restingstructures and improved heat conduction. Solarized plotswere covered with 30-mm-thick transparent polyethylenefilm ($ 88% total visible transmittance and 20% infraredradiation [IR] absorption) from July 16, 2002, to September12, 2002, and from July 10, 2003, to September 9, 2003.Nonsolarized soil was similarly tilled and watered.

Soil Temperature Measurement

During solarization, the soil temperature was recordedcontinuously (every 30 min) at depths of 5 and 15 cm,using thermistors buried in the center of the plots (solarizedand nonsolarized) and connected to a portable digital mi-croprocessor.1

Plant Material and Management Practices

Five-week-old tomato transplants (‘Ikram’ F1, Syngenta)were planted on October 2, 2002, and October 7, 2003,with a within-row planting distance of 0.4 m, and an in-terrow spacing of 1.15 m; this gave a density of 2.17 plantsm22. As the plants grew, lateral shoots were removed man-ually, and the resulting single stem was trained to the high-wire system. Plants were headed back after twelve trusses at114 (first season) and 125 (second season) d after planting(DAP). A fertigation program, commonly used in the areafor tomato crops, was adopted (24.4 g N, 18.5 g phosphoruspentoxide [P2O5], 26.2 of potassium oxide [K2O], 27.0magnesium oxide [MgO], and 0.4 g iron [Fe] per seasonper tomato plant). Drip irrigation was carried out when theaccumulated daily evaporation reached 25 mm, 100% ofmaximum evapotranspiration (ETP). Pest control followedstandard commercial practice. Bumblebees (Bombus terrestrisL.) were introduced into the greenhouse for improved pol-lination. The oldest tomato plant leaves were periodicallyremoved. Harvesting was carried out from January 16,2003, to May 5, 2003 (106 to 215 DAP), and from January29, 2004, to May 13, 2004 (114 to 219 DAP). No addi-tional heat, light, or carbon dioxide (CO2) was provided inthe greenhouse during the crop cycle.

Germination and Viability of Branched Broomrape

Mature branched broomrape seeds were collected in May2002 at the same location as the experiment, and 10-mgsubsamples were stored in the dark at room temperature (18to 25 C). Seeds were placed in 0.15-mm by 0.15-mm fine-mesh, nylon gauze bags, and on the day before the treatmentinitiation, bags were buried at 5 and 15 cm depth in eachplot. One day after removing the polyethylene covers, allbags were recovered from the soil, the branched broomrapeseed was removed, and germination and viability tests werecarried out. For the germination test, 250 seeds were placedin a 9-cm Petri dish on one piece of filter paper (WhatmanNo. 33) with 5 ml of stimulant solution and incubated inthe dark at 18 6 1 C. The stimulant solution was preparedby dissolving 10 mg of the synthetic germination stimulantGR242 (Johnson et al. 1981; Zwanenburg et al. 1986) in10 ml of acetone and diluting 1,000-fold with a 0.3-mMbuffer of 2-(N-morpholino) ethanesulfonic acid (MES)4,pH 6.1. Emergence was recorded under a stereomicroscopeat 3-d intervals until no more germination occurred. Whenthe germ tube was at least as long as its width (90 to 130mm), seeds were considered to have germinated and wereremoved.

The seed viability test was carried out by slightly modi-fying the procedure suggested by Khalaf (1991). Five mil-ligrams of seeds were submerged for 5 min in a 6% sodiumhypochlorite solution to bleach the dark seed coat, then re-peatedly washed in distilled water, dried in a flow of air at

Mauromicale et al.: Solarization for controlling of Orobanche ramosa • 879

TABLE 1. Number of days when soil temperature was $ 40, 45, 50, or 55 C during the solarization period at two soil depths.

Treatment

5 cm

$ 40 C $ 45 C $ 50 C $ 55 C

15 cm

$ 40 C $ 45 C $ 50 C $ 55 C

2002SolarizedNonsolarized

521

340

80

00

380

30

00

00

2003SolarizedNonsolarized

6253

5820

530

140

610

230

00

00

40 C, and imbibed on Whatman paper No. 1 in 6-cm-diamPetri dishes. In each dish, 3 ml of a 1% solution of 2,3,5-triphenyltetrazolium chloride (TTC)5, prepared followingInternational Seed Testing Association (1996) rules, wasadded, and the dish was incubated in the dark at 25 C for72 h. Red or pink seeds were considered viable, whereasthose that were not colored were considered dead (modifiedfrom Linke 1987). Seed viability was assessed using a bin-ocular dissecting microscope.

Collection of Biological and Production Data inthe Greenhouse

Branched Broomrape

The intensity of parasite infestation was evaluated bycounting, seven times per season, between mid-Novemberand May, the number of emerged branched broomrapeshoots per tomato plant. Branched broomrape shoots fromfour tomato plants for each plot were collected by hand inmid-April (both seasons) and weighed. In addition, at cropharvest, all tomato roots of plants grown in solarized soilwere collected to record the presence of branched broomrapehaustoria and underground tubercles.

Tomato Crop

In both seasons, four aboveground plant samples werecollected in mid-April, when the crop had reached its max-imum growth rate, and fresh weight of leaves and stems wasdetermined. Over the harvest period (from 106 to 215 DAPand from 114 to 219 DAP), the number and weight of ripefruits harvested from 10 plants plot21 were recorded.

Statistical Analysis

Biological and production parameters were subjected toANOVA6 where appropriate and mean separations weremade following Fisher’s protected LSD test. Regression anal-yses between branched broomrape infestation and tomatoyield (and its components) were also performed.

Temperature During the Crop Growth

Over the period of the crop cycle from October to earlyMay, mean temperatures in the greenhouse maxima andminima (in C) for the two seasons were 32.0 and 33.0 and22.8 and 21.3, respectively.

Results

Soil Temperature

Solarization substantially increased the soil temperature inboth seasons and at both depths. The highest recorded ab-solute maximum temperatures at 5 cm depth in mulchedsoil were 51.4 and 55.8 C in the first and second seasons,respectively, compared with 40.3 and 46.5 C in bare soil.The number of days when the maximum soil temperatureequaled or exceeded 40, 45, 50, and 55 C at depths of 5and 15 cm is shown in Table 1. Significantly, a temperatureabove 458C at 5 cm was recorded for 34 (first season) and58 (second season) d in solarized but for 0 (first season) and20 (second season) d in nonsolarized soil (Table 1). At 15cm, a temperature above 45 C was recorded for 3 (firstseason) and 23 (second season) d only in solarized soil (Ta-ble 1). The diurnal fluctuation in soil temperature at 5 and15 cm is illustrated in Figure 1.

Branched Broomrape Control

In both years, branched broomrape was completely con-trolled by soil solarization because the treatment did notallow the development and emergence of shoots, under-ground haustoria, or tubercles on the tomato roots. In con-trast, in nonsolarized soil, branched broomrape shoots hademerged by 45 DAP (first season) and 56 DAP (secondseason), and by 86 DAP (95 DAP), there were as many as43 (52) shoots per tomato plant (Figure 2). At the end ofthe 2002 and 2003 cropping seasons, the number ofbranched broomrape shoots per tomato plant peaked at 133(6 23) and 316 (6 21) with a fresh weight of 125 g (611) and 173 g (6 8), respectively.

Germination of branched broomrape seed sown at 5 and15 cm was zero in solarized soil, whereas it reached 83 and81%, respectively, in nonsolarized soil. The viability of bur-ied seed at 5 and 15 cm was about 93% in nonsolarizedsoil but only 2% and 6% in solarized soil, respectively. Noparasites other than branched broomrape were found on thetomato roots in either the solarized or the nonsolarized soil.

Tomato Plant Growth and Fruit Yield

Plant growth and fruit yield were consistently and sig-nificantly higher in solarized soil than in nonsolarized soil.In mid-April, when the tomato plant reached its maximumsize, soil solarization increased fresh leaf and stem weightper plant (Figure 3). Yield rate and components of fruityield over the harvest time were strongly and significantly

880 • Weed Science 53, November–December 2005

FIGURE 1. Diurnal trends of soil temperature in solarized and nonsolarized soil. Each symbol represents the half hourly mean temperature for the entireperiod of soil solarization.

affected by soil solarization (Figures 4–6). In both seasons,fruit yield in solarized and nonsolarized plots was similarat the first harvest (106 DAP and 114 DAP), whereas start-ing with the second harvest, the yield rate of plants grownin solarized soil was significantly higher than for plantsgrown in nonsolarized soil (Figure 4). At the beginning ofApril, the differences in yield between solarized and non-solarized plots had already reached 77% (3.9 vs. 2.2 kgplant21, first season) and 125% (3.6 vs. 1.6 kg plant21,second season). At the end of the harvest, plants grown insolarized soil produced 5.6 (6.8) kg plant21, comparedwith 2.4 (1.9) kg plant21 from plants grown in nonsolar-ized soil, equivalent to a yield increase of 133 and 258%,respectively (Figure 4). The yield differences between thesolarized and nonsolarized treatments during the harvestperiod were delivered largely by the number of fruit perplant rather than average fruit weight (Figures 5 and 6).Plants grown in solarized soil produced 61.5 (75.8) fruitsper plant, with an average fruit weight of 86.4 g (102.6g), whereas plants grown in nonsolarized soil produced31.5 (26.4) fruits per plant with an average weight of 66.3g (77.7 g), respectively. Tomato fruit yield (and its com-ponents) and infestation severity of branched broomrapewere negatively correlated (P , 0.001), as predicted (seethe captions to Figures 4–6).

Discussion

Under the Mediterranean conditions of southern Italy,soil solarization proved to be an excellent method for com-plete control of branched broomrape infestation. In addi-tion, solarization was able to consistently improve tomatoyield under greenhouse conditions, where branched broom-rape is particularly destructive (Hodosy 1981; Qasem 1998;Qasem and Kasrawi 1995). Without solarization treatment,branched broomrape consistently decreased fruit yield. Asthe severity of the infestation increased (over the period ofmid-December to May), the growth of tomato plants wasincreasingly inhibited. The incidence of chlorosis increased,the photosynthetic rate was reduced (data not shown), andplants were visibly witted in the middle of the day, leadingto a yield collapse as early as mid-spring. Fruit yield and itscomponents were negatively and significantly correlatedwith the number of branched broomrape shoots per tomatoplant. Regression analysis associated 85 and 66% of the var-iation in tomato yield with the severity of the branchedbroomrape attack for 2002 and 2003 tomato crops, respec-tively.

Soil solarization provided total control of branchedbroomrape because shoot emergence from treated soil wascompletely inhibited, and no haustoria or underground tu-

Mauromicale et al.: Solarization for controlling of Orobanche ramosa • 881

FIGURE 2. Number of emerged branched broomrape shoots during twogrowing seasons in nonsolarized soil. Note the failure of shoot emergencein solarized soil. Bars represent standard errors.

FIGURE 3. The effect of soil solarization on the fresh weight of tomato plantparts in mid-April averaged over the two crop seasons (***, significant dif-ference at P # 0.001).

FIGURE 4. The effect of soil solarization on tomato yield accumulation undergreenhouse conditions. Regression equation relating fruit yield accumula-tion at end harvest to infestation severity (number of emerged broomrapeper tomato plant) was y 5 5.3 2 0.023x, r 5 0.919***, R2 5 0.845 forthe 2002 to 2003 season; and y 5 5.9 2 0.011x, r 5 0.810***, R2 50.656 for the 2003 to 2004 season (*, **, ***, and NS are significantdifferences at P # 0.05, 0.01, 0.001, and not significant, respectively).

bercles were found on the tomato roots at the end of thecrop cycle. The high soil temperature attained by mulchinginhibited branched broomrape germination killing about95% of the buried seed and inducing secondary dormancyin the remaining 5%. This result is important because itindicates that the soil seedbank of branched broomrape seedshould be reduced after each solarization, and we predictthat a number of consecutive solarizations will result in lim-iting parasite seed number in the soil to a level where normaldevelopment of the tomato crop is not compromised. Fieldtrials are planned to assess the degree of viability of branchedbroomrape seeds buried naturally in the soil after varioussolarization treatments because we have previously demon-strated that the exposure of crenate broomrape seeds to hightemperatures led to a significant progressive reduction ingermination and a linear decrease in seed viability (Maurom-icale et al. 2000).

Soil solarization improved tomato plant growth and, con-sequently, fruit yield. The latter was 133 6 9 and 258 618% higher than in nonsolarized soil each season, respec-tively. Furthermore, yield levels were 68% (first season) and104% (second season) above the average official greenhousetomato yield in Italy (ISTAT 2003–2004). These remark-able increases in tomato yields by soil solarization are largelyattributable to the absence of branched broomrape infesta-tion, but we cannot exclude additional beneficial effects gen-

882 • Weed Science 53, November–December 2005

FIGURE 5. The effect of soil solarization on tomato fruit number accumu-lation under greenhouse conditions. Regression equation relating total num-ber fruit per plant to infestation severity (number of emerged broomrapeper tomato plant) was y 5 58.9 2 0.197x, r 5 0.814***, R2 5 0.747 forthe 2002 to 2003 season; and y 5 67.4 2 0.107x, r 5 0.787***, R2 50.620 for the 2003 to 2004 season (**, ***, and NS are significant differ-ences at P # 0.01, 0.001, and not significant, respectively).

FIGURE 6. The effect of soil solarization on tomato average fruit weight ateach harvest under greenhouse conditions. Regression equation relating thefruit average weight, across harvest, to infestation severity (number ofemerged broomrape per tomato plant) was y 5 90.9 2 0.154x, r 50.860***, R2 5 0.740 for the 2002 to 2003 season; and y 5 87.1 2 0.047x,r 5 0.877***, R2 5 0.770 for the 2003 to 2004 season (*, **, ***, and NSare significant differences at P # 0.05, 0.01, 0.001, and not significant,respectively).

erated by the solarization treatment, such as the control ofsoil-borne diseases, an increased release and uptake of mac-ro- and micronutrients, the release of plant growth regula-tors, the enhancement of mycorrhizal growth, and an in-crease in endogenous gibberellin supply (Chen and Katan1980; Chen et al. 1991; Grunzweig et al. 2000; Maurom-icale et al. 2005). Given the high correlation between yieldand branched broomrape infestation, as well as the absenceof soil-borne pathogens, and the optimal plant nutritionmaintained over the crop cycle, the additional beneficial ef-fects provided by soil solarization are probably minor com-pared with the negative effects of branched broomrape pop-ulations.

At present, branched broomrape control in greenhousesin the Mediterranean basin and elsewhere is commonly con-trolled by regular preplant soil fumigation with methyl bro-mide; however, the use of this fumigant will be phased outby 2015 (2005 in the European Union). Therefore,branched broomrape attack is currently a significant risk.Where legume cropping has been abandoned because ofhigh Orobanche infection and low levels and stability of yield(Foti 1994; Mesa-Garcia and Garcia-Torres 1986), the

adoption of soil solarization may be able to rescue theseproduction areas. There are advantages to using solarization:specifically, it is a simple, nonchemical, nonhazardous meth-od that avoids the use of any toxic materials, does not con-taminate the site, and is, therefore, suited to organic farmingor other low-input agricultural systems. As global environ-mental quality considerations grow in importance, alongwith an increasing human population, evolving concepts,such as soil solarization and other uses of solar energy inagriculture, will become more important (Stapleton 2000).

Further research is necessary to determine the degree ofbranched broomrape seedbank viability down the soil profileand its relationship with soil temperature reached duringsolarization to facilitate strategies to completely eradicate theparasite weed from the soil.

Sources of Materials1 Thermistors and Portable digital HI 9284C microprocessor,

Hanna Instruments s.r.l., Via E. Fermi 10, Sarmeola di Rubano(Padova) 35030, Italy.

2 GR24, supplied by Binne Zwanenburg, Department of Or-

Mauromicale et al.: Solarization for controlling of Orobanche ramosa • 883

ganic Chemistry, NSR-Center for Molecular Structure, Design andSynthesis, University of Nijmegen, Toemooiveld, 6525 ED Nij-megen, The Netherlands.

3 Whatman International Ltd, Springfield Mill, Sandling Road,Maidstone, ME14 2LE, U.K.

4 2-(N-morpholino) ethanesulfonic acid (MES), Sigma-Aldrichs.r.l. Via Gallarate 154, Milano 20151, Italy.

5 2,3,5-triphenyltetrazolium chloride (TTC), Sigma-Aldrich s.r.l.Via Gallarate 154, Milano 20151, Italy.

6 CoStat—Statistics Software version 6.003, CoHort Software,798 Lighthouse Ave. PMB 320, Monterey, CA 93940.

Acknowledgments

The authors thank the Azienda Agricola Fratelli Giardina forhaving hosted the experiment in their greenhouses and for theirgenerous help in carrying out the trials and Mr. Angelo Litrico forexcellent technical assistance.

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Received March 1, 2005, and approved July 25, 2005.