ALTERNATIVES TO METHYL BROMIDE FOR THE MANAGEMENT OF
SOIL-BORNE PLANT PATHOGENS IN CYPRUS
N. IOANNOU
Agricultural Research Institute, Plant Pathology
and Biotechnology Section, 1516 Nicosia, Cyprus
I. Introduction
The main uses of methyl bromide (MB) in Cyprus are for soil fumigation in vegetable, strawberry and ornamental
production. The total acreage of these crops in the Government-controlled area of the Island is about 4,100 ha, of which about
16% represent crops grown under protected cultivation (1). The intensive production systems employed by growers,
especially monoculture and year-round cultivation, favour the quick build-up of high inoculum densities of soil-borne
pathogens. Management of these pathogens, especially under protected cultivation, is based primarily on pre-plant soil
fumigation with MB and occasionally with other soil fumigants. Soil fumigation is usually supplemented by additional plant
protection products (mainly systemics) applied after planting through the irrigation system. The need to protect high value
crops from damage caused by soil-borne pathogens, frequently leads growers to excessive application of chemicals, with
negative effects on humans, animals, plants and the environment (2, 10, 113), including:
a) Eradication of the beneficial soil microflora and microfauna, resulting in elimination of natural biological control and
resurgence of secondary pests and diseases. The “biological vacuum”, on the other hand, created by the use of potent
biocides, such as MB, is usually responsible for the quick re-infestation of treated soils.
Toxic side-effects on humans, plants (phytotoxicity) and other “non-target” organisms.
Pollution of the environment, including soil, water and the atmosphere. MB, in particular, is considered a major pollutant of
underground water and has been implicated in the depletion of the ozone layer.
Pesticide residues in agricultural products, creating health risks for the consumers and major obstacles to the international
agricultural trade. Soil fumigation with MB, in particular, is known to leave bromine residues in soil, which can be taken up
by plants and accumulate in leaves. Because of this, problems with bromine residues in leafy vegetables, such as lettuce, are
quite common.
MB is a powerful soil fumigant providing effective control of a wide range of soil-borne pathogens and pests, including
fungi, bacteria, nematodes, insects, mites, weeds and parasitic plants. It is also relatively economic and convenient in its use.
Despite these major advantages, the use of MB has been associated with major problems, including the depletion of the ozone
layer (2). Because of this, its production and use will be phased out on a world-wide scale, by 2005 in the E.U. and other
developed countries and by 2015 in the developing countries (Montreal Protocol). Therefore, there is an urgent need to define
and implement alternative solutions for managing soil-borne pathogens (10). For Cyprus and the rest of the southern
European and Mediterranean region, the most appropriate alternative appears to be the use of soil solarization, alone or in
combination with other control methods, in the context of integrated pest management (IPM). To this end, a research program
focusing on soil solarization was undertaken during the last decade by the Plant Pathology Laboratory of the Agricultural
Research Institute (ARI) of Cyprus. In order to improve the effectiveness of solarization, and thus shorten the normally long
duration of the treatment, various modifications of the basic technique and combinations with other methods, including
resistant cultivars, resistant rootstocks, pesticides, soil additives and organic soil amendments, are studied. The work is
centered on three major vegetable crops, namely tomato, watermelon and eggplant, grown under both protected and
unprotected cultivation. Results obtained so far are briefly reviewed in this paper.
II. Experiments with tomato
Tomato is a major vegetable crop in Cyprus, cultivated the year round in greenhouses, under low tunnels, and in the open
field. Trends towards monoculture and intensive cropping practices employed by growers have increased losses from soilborne diseases and pests, including: a) vascular wilts caused by Fusarium oxysporum f. sp. lycopersici (FOL) and
Verticillium dahliae; b) corky root rot caused by Pyrenochaeta lycopersici; c) root-knot nematodes (Meloidogyne spp.); and
d) weeds and parasitic plants (Orobanche sp.).
For the control of these pathogens the following studies were carried
out in various tomato production areas of Cyprus (3,4).
1. Wilt-resistant cultivars
Two of the three known races of FOL (races 1 and 2) and one of the two known races of V. dahliae (race 1) were identified
(Ioannou, unpublished). Resistance to these three races, designated as VF 1F2 or VF2, is found in many new tomato hybrids,
suitable for both open-field and greenhouse production. Resistant cultivars can therefore be a major means of Fusarium and
Verticillium wilt control in Cyprus. Other forms of resistance, like V, F or VF, provide only partial protection from wilt
diseases, and their use is not normally recommended under Cyprus conditions. FOL race 3 and V. dahliae race 2, known to
exist in other parts of the world, have not been detected in Cyprus yet.
Soil solarization in the open field
Two field trials were carried out in order to investigate the use of soil solarization for tomato production in the open field (3).
Solarization treatments, applied in 80 cm wide strips for 7-8 weeks in July-August, raised the maximum soil temperature by
10-11oC, reduced the population density of Fusarium spp. in soil by 88-93%, and provided effective control of Fusarium and
Verticillium wilt diseases on tomato. It also controlled weeds by 90%, improved tomato plant growth, and increased fruit
yield by 60-135%, compared to the untreated check. One heavy irrigation (100 mm) at the beginning of solarization
apparently provided sufficient moisture for the duration of the treatment, as supplementary irrigations during the solarization
period did not appreciably augment its effectiveness (3,5). Solarization appeared to be an effective, economic and
environmentally friendly soil disinfestation method, that could readily replace ΜΒ fumigation in the open field.
3. Soil solarization under greenhouse conditions
The possibility of using soil solarization as an alternative to MB was examined in four greenhouse tomato trials (4).
Solarization was applied for 8 weeks in July-August and compared to MB fumigation applied in September, before planting,
at 80 g/m2. Both methods provided effective control of Fusarium wilt and corky root rot on tomato plants. MB fumigation
was in addition highly effective against root-knot nematodes, whereas nematode control with solarization did not exceed
50%. Both treatments, however, resulted in similar fruit yield increases, ranging within 90-140% compared to plants grown
in untreated soil.
During the second cropping season following soil treatment, solarization exhibited two times higher residual effect on
vascular wilt diseases compared to MB fumigation. The latter treatment, however, was superior to solarization in its residual
effect on root-knot nematodes and to a lesser extent on corky root rot. Fruit yields from solarized and MB-fumigated soil
during the second cropping season were higher than those obtained from untreated soil by about 35% and 60%, respectively
(4). In conclusion, solarization appears to be an effective alternative to MB fumigation in greenhouse tomato production,
especially if integrated with other approaches enabling more effective nematode control.
4. Soil solarization integrated with other methods
Trials carried out at Zigi Experimental Station during the last two years aim to evaluate solarization treatments of varying
duration (2-8 weeks) in combination with various soil pesticides, biological control agents, natural products containing plant
extracts, organic soil amendments etc. The objective is to improve the effectiveness of solarization, especially against
nematodes, and thus enable reduction of its duration in order to make it more integratable with intensive production schedules
presently employed by tomato growers. Some of the products and methods evaluated in combination with soil solarization
include:
a) The fungus Paecilomyces lilacinus for biological control of nematodes.
b) The commercial product “Nemaclean” containing plant extracts.
c) Addition of chitin to the soil, together with sulfur and Thiobacillus spp., in the form of the commercial product “Acidam”
Cultivars combining resistance to nematodes, vascular wilts and other soil-borne pathogens.
Preliminary data so far indicate that at least some of the above treatments can correct or alleviate the main weakness of
solarization, i.e. its reduced effectiveness against nematodes. Such a development would encourage the adoption of
solarization by growers.
5. Fusarium root and crown rot of tomato
During the last two growing seasons a new soil-borne disease of tomato,characterized by root and crown rot symptoms, was
recorded in several greenhouses in Limassol district (Parekklesia area). The causal agent was identified as Fusarium
oxysporum f.sp. radicis-lycopersici (FORL) by vegetative compatibility tests (carried out in cooperation with Dr. T. Katan at
the Volcani Center, Israel) and by comparative pathogenicity tests in vitro and in vivo. Although still of limited distribution
this disease is potentially very damaging to tomato crops because:
a) It attacks all Fusarium – resistant cultivars
b) it is only partially controlled by soil fumigation or soil solarization, apparently because treated soils can be quickly reinfested by air-borne conidia produced externally at the basal stem of infected plants.
Trials presently in progress investigate various forms of chemical control in combination with growth regulators and plant
nutrition products aiming to encourage the production of new roots, which would enable the survival of infected plants. In
practice, however, the only control measures presently recommended are soil solarization, in combination with roguing of
infected plants and adequate heating of greenhouses. The latter measure is helpful since FORL is favored by low
temperatures and it is most damaging in unheated greenhouses.
III. Experiments with watermelon
Fusarium wilt of watermelon caused by Fusarium oxysporum f. sp. niveum (FON) is the most important limiting factor for
watermelon production in Cyprus (6, 7, 8, 9, 11, 12). During the 1980s efforts were made to control the disease by strip
application of soil solarization or MB fumigation, with varying results (6, 11). In recent years, a new research effort was
undertaken aiming on one hand to improve the effectiveness of solarization with various soil treatments and on the other to
investigate the use of resistant cultivars or resistant rootstocks (8, 9, 12):
1. Solarization and other soil treatments
In trials carried out during the 1980s, soil solarization and MB fumigation, applied separately in 1-m-wide strips, gave only
partial control of Fusarium wilt, which was satisfactory only in lightly infested soils (6,11). For heavily infested soils there
was clearly a need to improve the effectiveness of the treatment (8, 12). Such an improvement was pursued through various
modifications of the basic solarization technique and combinations with other methods, including:
Increasing the width of the solarization strip from 1 to 2 m.
Solarization with a double rather than a single polyethylene sheet (strips of 1 or 2 m width).
Addition of ammonium fertilizers in the soil (120-240 kg N/ha) before solarization.
Combined treatments of soil solarization for 6 weeks in July-August, followed by MB fumigation at 40 or 80 g/m2 in March,
just before planting.
The first two modifications (2-m-wide strips and double sheet) improved the effectiveness of solarization and increased yield,
but differences were not significant. The addition of ammonium fertilizers, however, improved significantly the level of wilt
control and increased marketable yield by 40-140% over that obtained with solarization alone. The low N rate (120 kg/ha)
was almost as effective as the high rate (240 kg/ha). Ammonium sulfate and monoammonium phosphate were equally
effective, but urea was ineffective. The addition of fertilizer alone (without solarization) had no effect at all.
The
mode of synergistic action of ammonium fertilizers with soil solarization is believed to be through the production of
ammonia gas (due to high soil temperatures) which acts as a mild disinfestant against soil-borne pathogens.
A significant improvement of the level of wilt control was also obtained with the combined soil solarization – MB fumigation
treatments, which increased marketable yield by 42-91% over that of soil solarization alone. The low rate of methyl bromide
(40 g/m2) was as effective as the normal rate used by growers (80 g/m2) (8,12).
2. Identification of local races of FON and cultivar reaction
Trials with 35 reportedly resistant watermelon cultivars showed that all were susceptible to the local isolates of FON (7,11).
In order to identify the prevailing FON races in Cyprus, pathogenicity tests were carried out on three differential cultivars,
using 20 local isolates of unknown race designation, in comparison with isolates from USA and Israel, known to belong
to races 0,1 and 2. The majority of local isolates were identified as race 2, a highly aggressive biotype able to attack all
known resistant cultivars (9,12). A source of resistance to race 2 has been identified but so far it has not been incorporated
into commercial cultivars.
3. Grafting on resistant rootstocks
In view of the susceptible reaction of all resistant cultivars to local FON isolates of race 2, efforts to control wilt were
directed towards the use of resistant rootstocks on which susceptible watermelon cultivars would be grafted (9,12). Several
local cucurbit species and imported commercial rootstocks were evaluated in the laboratory for resistance to FON and for
compatibility with the main watermelon cultivars. Ten prospective rootstocks were pre-selected and subsequently evaluated
in field trials, with the following results:
a) All rootstocks provided 100% protection from FON, but Cucurbita maxima (local) and C. ficifolia (imported) were
susceptible to Rhizoctonia solani and Pythium spp.
The growth and yield of grafted plants were greatly improved compared to ungrafted controls, while fruit quality was not
affected in any way by grafting. The yield of grafted Crimson Sweet watermelon reached a record level of 150 tons/ha.
The most promising rootstocks among introduced ones were the RS841 F1 and Early M F1, and among local ones were the
Lagenaria siceraria “clavata”, L. siceraria “rodunta” and Cucurbita pepo “melopepo”.
Although growing grafted watermelon represents a novel horticultural practice for Cyprus, the technique has been quickly
and widely adopted by growers. Presently, over 80% of watermelons grown in the open field and under low tunnels are
grafted on various rootstocks. Grafted plants are produced by fully equipped commercial nurseries.
During the last three years research efforts have been directed towards the utilization of wilt-resistant rootstocks for offseason watermelon production in heated greenhouses. Although there are still many technical aspects that need further
investigation, results so far are quite promising since this method enables watermelon production as early as March, when
prices are very high.
Integrated management of soil-borne pathogens
Fusarium – resistant rootstocks are susceptible to other soil-borne pathogens, including V. dahliae, Rhizoctonia salani,
Pythium spp. etc., which at present are still of minor importance (9,12). With the wide cultivation of grafted watermelons,
however, there are indications that the importance of these pathogens will gradually increase. Therefore, research efforts are
presently directed towards the integrated management of all soil-borne pathogens of watermelon through the combined
application of different control methods, including soil solarization, organic soil amendments, fertilizers, natural products,
and grafting on resistant rootstocks.
IV. Experiments with eggplant
Eggplant is a very popular fruit vegetable in Cyprus, cultivated the year round in greenhouses, under low plastic tunnels and
in the open field. Under all cultivation systems, eggplant crops sustain severe losses from soil-borne diseases, especially
Verticillium wilt caused by V. dahlilae, corky root rot caused by Pyrenochaeta lycopersici, and root-knot nematodes
(Meloidogyne spp). All commercial eggplant cultivars presently available are susceptible to these pathogens and, therefore,
their management is almost exclusively based on MB fumigation. In tomato, however, most commercial cultivars, including
few rootstock varieties, possess multiple resistance or tolerance to soil-borne pathogens. The possibility of grafting
susceptible eggplant cultivars on a resistant tomato rootstock (Brigeor F1, obtained from INRA, France) was investigated
with or without soil solarization, in trials carried out in the open field and under greenhouse conditions (5). The results could
be summarized as follows:
a) Soil solarization was highly effective against Verticillium wilt but only partially effective against corky root rot and rootknot nematodes; it also controlled adequately most annual weeds.
By contrast, grafting provided complete protection from corky root rot and root knot, but only partial protection from
Verticillium wilt. Complete resistance to nematodes, however, was exhibited only in trials with greenhouse-grown (winter)
crops. In open-field (summer) crops, about 50% of the grafted plants sustained slight nematode infection, apparently because
of resistance break- down due to high soil temperatures.
The combined application of solarization and grafting was much more effective than either method alone, as the two
integrated methods complemented each other, providing complete protection from all three diseases. Most important, the two
methods combined had an additive effect on yield, resulting in a significant increase over those obtained by either method
alone. Thus, the average yield (kg/plant) obtained in two greenhouse trials was 9.5 for the control, 16.1 for grafting alone,
14.1 for solarization alone and 20.2 for the combination of the two methods.
V. Conclusions
Tomato
Results obtained so far indicate that the use of MB in tomato production can be readily replaced by soil solarization, applied
either in strips for open-field and low-tunnel crops or as overall treatment for greenhouse crops. Depending on particular
pathogens involved, soil solarization can be integrated with one or more of the following methods, in order to augment its
effectiveness and enable reduction of its duration:
a) Tomato cultivars combining VF1F2 type of resistance to vascular wilt diseases
b) Nematode-resistant cultivars
c) Application of conventional chemical nematicides
Use of biological control agents or natural products, directed primarily against nematodes and other pathogens.
2. Watermelon
At present the use of resistant rootstocks appears an excellent alternative, which has already replaced MB to a great extent.
However, in view of the threat of new emerging soil-borne diseases, MB substitution should not be based solely on resistant
rootstocks but rather on the integrated use of all control methods presently available, including: soil solarization, chemical,
natural and biological soil additives, resistant rootstocks and resistant varieties, if and when commercially available.
3. Eggplant
Neither solarization nor grafting on resistant tomato rootstocks, alone, can provide suitable MB substitutes for eggplant
production. The integrated use of the two methods, however, appears to be a sustainable alternative to MB, both for crops
grown in the open field and for greenhouse-grown crops.
Acknowledgements
This article reviews the results of research on alternatives to methyl bromide carried out at the Agricultural Research Institute
of Cyprus during the last decade. I wish to express my sincere appreciation to the technical staff of the Plant Pathology and
Biotechnology Section and in particular to Mrs Artemis Hadjinicoli and Messrs A. Hadjinicolis, Chr. Chrysostomou, D.
Constantinou and N. Loizias for skillful technical support, without which this work would not have been possible. Special
thanks go to Mr. Constantinos Poullis, who as a Ph.D. candidate undertook most of the responsibility for research work on
Fusarium wilt of watermelon.
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