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Pathogens
  • Review
  • Open Access

28 January 2021

Can Anaerobic Soil Disinfestation (ASD) be a Game Changer in Tropical Agriculture?

and
1
Department of Plant and Molecular Biology, University of Kelaniya, Kelaniya 11600, Sri Lanka
2
Department of Multidisciplinary Studies, Faculty of Technology, Eastern University, Batticaloa 30376, Sri Lanka
*
Author to whom correspondence should be addressed.
This article belongs to the Special Issue Biological Control of Phytopathogens: Mechanisms and Applications

Abstract

Anaerobic soil disinfection (ASD) has been identified as an alternative soil-borne pathogen control strategy to chemical fumigation. ASD involves the application of an easily liable carbon source followed by irrigation to field capacity and maintenance of an anaerobic condition for a certain period. A literature search undertaken on ASD found that more than 50 comprehensive research projects have been conducted since its first discovery in 2000. Most of these studies were conducted in the USA and in the Netherlands. Though the exact mechanism of ASD in pathogen control is unknown, promising results have been reported against a wide range of pathogens such as fungi, nematodes, protists, and oomycetes. However, it is interesting to note that, except for a few studies, ASD research in the developing world and in the tropical countries has lagged behind. Nevertheless, with soil quality depletion, reduction in arable lands, and exponential population growth, a drastic change to the current agricultural practices should be adapted since yield gain has reached a plateau for major staple crops. Under such circumstances, we identified the gaps and the potentials of ASD in tropical agricultural systems and proposed promising biodegradable materials.

1. Introduction

Crops are often attacked by various plant pathogens, plant-parasitic nematodes, insect pests, and weeds causing great economic losses around the world. Among diverse groups of plant pathogens, soil-borne phytopathogens pose a great threat to crop production [1,2,3]. Although soil is a home for billions of living organisms (both macro and microorganisms), they must face a multitude of challenges such as flood, drought, and agricultural practices. However, soil-borne pathogens can survive under these challenges and cause serious crop damage around the world. For example, waterlogged agricultural fields may be unfavourable for many organisms but favourable for root-infecting fungi and oomycetes such as Pythium and Phytophthora spp. [4,5,6]. Although drought conditions are unfavourable for most of the organisms, soil-borne pathogen species such as Fusarium spp. and Verticillium spp. [5] manage to cause severe infections. Hence, soil-borne phytopathogens show a great deal of evolutionary adaptations. They can survive in the soils for many years in the absence of host plants through the formation of resistant structures such as microsclerotia (Verticillium spp.), sclerotia (Sclerotinia spp.), chlamydospores (Fusarium spp.), or oospores (Phytophthora spp.) [7,8,9,10]. Microsclerotia and sclerotia have the same anatomical structure, consisting of outer melanized parenchyma cells and inner colorless medullary cells, and are asexual in nature. Chlamydospores are thick-walled asexual survival structures whereas oospores are thick-walled sexual structures with food reserves for better survival. These structures may be melanised or non-melanised. Melanisation of survival structures has several evolutionary advantages such as protection from UV radiation, successful penetration during infection, long-term survival, growth, and development [11,12]. Wilhelm [13] found the persistence of microsclerotia of Verticillium alboatrum for 14 years in soil, which were viable even after the exposure to desiccation at high temperatures. Ben-Yephet et al. [14] reported the survival of sclerotia of soil-borne Sclerotinia sclerotiorum declined after an outbreak of lettuce drop, nevertheless, about 5.5% were viable even after seven years. Babadoost and Pavon [15] assessed the survival of Phytophthora capsici oospores in the soil in Illinois (USA) and found three to four years of survivability. Apart from soil-borne fungal plant pathogens, plant-parasitic nematodes have been recognized as another group of challenging pathogens to manage [16].
Besides, each plant can be infected by several pathogen species and the complex nature of the soil environment, it is difficult to control diseases caused by soil-borne pathogens. Hence, successful control of soil-borne pathogens is a major challenge due to inherent difficulties of disease prediction, early detection, and accurate diagnosis [2]. Some modern crop production systems are based on raised-bed, plasticulture, and limited or short crop rotation-lengths, probably with the unavoidable application of broad-spectrum soil fumigants to manage pests and diseases [1]. Since the mid-20th century, synthetic chemicals have been used to control many plant diseases including a broad spectrum soil fumigant, methyl bromide (MeBr) [17,18,19]. Since then, MeBr has been heavily applied worldwide primarily to control soil-borne pathogens as well as the nematodes [20]. For example, five million kg of MeBr were used only in California in the year 2000 [21]. MeBr has been identified as a stratospheric ozone-depleting component by the U.S. Environmental Protection Agency (EPA) and the United Nations Environment Program (UNEP). Bolstered by the 1994 UNEP Montreal Protocol on Substances that Deplete the Ozone Layer, MeBr was identified as a major ozone-depleting compound [22]. Thereafter, MeBr was completely banned by the 1 January 2005 with few exceptions [19,21,23,24].
Alternative synthetic fumigants such as 1,3-dichloropropene, 1,3-D, chloropicrin, trichloronitromethane, methyl isothiocyanate, allyl isothiocyanate (AITC), and dazomet were tested and applied by the farming communities around the world yet were poorly accepted due to geographic limitations, reduced efficacy, and regulatory constraints [25,26,27]. Moreover, many criticisms have been generated from the public and from the scientific communities against the use of such chemical soil disinfestation methods due to their toxicity on humans and undesirable effects on non-target organisms such as beneficial microflora, groundwater pollution, and development of resistance [19,28,29,30,31,32].
Therefore, farmers were compelled to use non-chemical approaches. Traditionally a number of environmental friendly approaches such as mixed cropping, crop rotation, resistant cultivars/selective breeding, application of biocontrol agents, flooding, solarisation, steaming, pasteurisation, hot water treatment, and bio-fumigation have been applied by farmers around the world to mitigate soil-borne diseases [19,33,34,35]. Nevertheless, these applications were not as popular as chemical fumigants due to several limitations [19]. Application of mixed cropping systems may be helpful in increasing the crop yield while addressing some of the soil-borne pathogen problems [36], yet it is not always economically feasible when the rotation is done with low economical value crops [35]. Although selective breeding shows some level of effectiveness against soil-borne pathogens, host resistance breakdown has been reported, and no completely resistant cultivars are available for all the crops [35]. Another option would be the use of biocontrol agents, however, these are highly specific for particular pathogen species if not for strains, and effectiveness is greatly dependent on the environmental factors [37]. Similarly, other non-chemical approaches have their own disadvantages, hence there have been limited applications [33,36,38,39,40,41].

Anaerobic Soil Disinfestation (ASD)

To minimize the above drawbacks of chemical and non-chemical methods of soil-borne pathogen control, researchers found alternative methods, and one such promising approach is anaerobic soil disinfestation (ASD), also called biological soil disinfection (BSD) or reductive soil disinfection (RDS). This method was first described independently by researchers in Japan [42,43] and in the Netherlands [44] and was later adapted to the USA [45] to control soil-borne pathogens in strawberry and vegetable fields. Thereafter, researchers around the world started applying this method, showing a great potential to control various soil-borne phytopathogens [44,45,46,47,48,49,50,51,52,53,54,55].
The method is characterized by non-chemical pre-plant control of soil-borne phytopathogens using few simple steps [29,56]. The first step of ASD is the incorporation of organic amendments (usually an easily labile carbon source) to the topsoil. The soil is later wetted to field capacity and covered with a clear (preferably black) and gas-impermeable polyethylene sheet for a defined period of time to maintain an anaerobic condition [57]. The effectiveness of ASD has been evaluated against soil-borne diseases such as potato brown rot [46], spinach and tomato wilt diseases [48], Prunus [58] and apple replant disease [50], Fusarium wilt of banana [59], root and crown rot diseases of pepper [60], etc., with promising results. ASD has now become popular in organic agriculture worldwide and is practiced under greenhouse and field conditions as well [47,51,61]. There is some evidence that ASD also can contribute to the development of disease-suppressive soils [57]. The objectives of this review were to thoroughly analyse all the studies conducted on ASD since its first discovery two decades ago, to discuss the current trends to identify the gaps of ASD research, especially emphasizing future research directions, and to discuss the potential use of ASD in the tropical agricultural systems.

2. Data Collection and Analysis

A thorough literature search was conducted from National Center for Biotechnology Information (NCBI), Google Scholar databases, and Mendeley referencing tool using the keywords anaerobic soil disinfection, biological soil disinfection, and reductive soil disinfection to filter studies conducted on these aspects during the past two decades. In this initial search, a total of 147,799 results were obtained. However, most of the outcomes were not directly relevant to our objectives, and the selection pipeline is shown in Figure 1. This literature was further analysed to extract information on study region, year, targeted pathogen, weed control, C source used, type of crop, duration of anaerobic period, type of mulch, crop yield improvement, etc. Review papers and duplicated, salami (fragmented publications) and irrelevant publications were excluded from the analysis. Finally, 56 complete, directly relevant, and original research publications originated in nine countries were included in the analysis. Some of these research papers have described ASD effect on more than a single pathogen species and in such instances, they were considered as two or more studies depending on the number of targeted pathogens. Therefore, final analysis was based on 109 studies published in 56 research papers.
Figure 1. Literature selection procedure. ASD—anaerobic soil disinfection; BSD—biological soil disinfection; RSD—reductive soil disinfection.

4. Challenges and Potentials of ASD as a Game Changer in the Tropics

The world’s population is estimated to reach over nine billion by 2050, which is roughly 34% higher than it is today, although the carrying capacity is just seven billion [93]. It is also predicted that the rapid population growth in the tropics and in developing countries is mainly responsible for this increase, and agriculture should be revolutionized to meet the increasing food demand [93,94,95]. It has been projected that future food production cannot be predicted by the historical grain yield patterns, and relative rate of grain yield may decrease in the future. In other words, yield gain has plateaued over time [96]. Therefore, it is obvious that developing countries, especially those in the tropics, might be adversely affected [97,98]. On top of that, 20–40% of worldwide agricultural crop productivity has been affected by pathogen and pest attacks and weeds, causing a considerable economic loss [99]. For example, in India, annual crop loss could reach up to USD 19 billion [100]. In addition to crop loss, arable land degradation is also a global concern. With industrialization and exponential population growth in the tropical developing countries, reduction of arable lands is inevitable, and it is the biggest threat to agricultural productivity. In addition, small-scale agricultural systems, multiple cropping systems, year-round crop availability, high level of crop diversity well as pathogen diversity, poor use of technology, low agricultural literacy among farmers, and low mechanization are some of the common characteristics of tropical, specially developing world agriculture [101]. Therefore, agricultural productivity in developing countries located in the tropics seriously lags behind than that of the temperate countries [102]. Hence, not only modernizing the agriculture but also soil health should be taken into account.
Interestingly, a majority of ASD studies have been carried out in temperate and sub-tropical regions. Of the studies reviewed, 63.3% were carried out in the USA. However, it has not been sufficiently applied or tested in the tropical regions, especially in the developing parts of the world where the agricultural system is completely different yet is the major income for a majority. Only one ASD study has been conducted each in Sri Lanka and in Nepal, and no records on ASD were found in other developing countries. The only ASD study conducted in Sri Lanka was published by our research group [55] and tested the ability of controlling soil-borne fungal pathogen, Sclerotinia sclerotiorum, using cabbage (Brassica oleracea) and leek (Allium ampeloprasum) cull piles, durian (Durio zibethinus) peels, and grass cuttings (Axonopus compressus) as C sources. During this pot assay, 60–100 mg g−1 of cabbage and leek cull piles were found to be effective in 100% mitigation of sclerotial germination. With the promising results of pot assay, field trials were conducted in Sri Lanka using leek, cabbage, and a mixture of leek and cabbage cull pieces at different rates as wet and dry applications. The highest mean sclerotial germination inhibition (96.66%) was associated with the application of wet leek cull pieces at the rate of 43.05 t ha−1 and dried cabbage cull pieces at the rate of 32.28 t ha−1 [103]. In a study conducted in Nepal, Bhandari et al. [104] reported the best control of clubroot disease of cauliflower caused by Plasmodiophora brassicae was achieved by the amendment of cheuri cake (Diploknema butyracea) as the C source, while molasses and rice bran treatments were ineffective. In addition, cheuri cake also increased the yield compared to the untreated control. Therefore, it seems that ASD with different C sources is a promising approach to achieve disease suppression and gain yield and improve soil condition in tropical soil and in developing countries as well. However, thorough studies are necessary targeting the tropical region since there is a severe information gap. One major limitation in ASD is the cost associated with the use of plastic/impermeable sheets, and it is estimated that ASD costs more than chemical fumigation [105,106]. In addition, labour cost and non-biodegradability of polyethylene are serious issues. However, when considering the long-term effects, it is a worthwhile investment, and polyethylene sheets can be reused/shared among farmers due to small scale agriculture. We found that, in traditional agricultural practices in Sri Lanka, farmers used to draw certain patterns on the ground near the fields to get vermivorous and insectivorous birds’ attention to the field so that pest attacks could be minimised (personal communication, traditional farmers in Dambulla and Polonnaruwa, Sri Lanka). With this information, we propose to use cover material with various patterns as another dimension to the ASD research. However, the higher cost of plastic and labour appear to be the major limitations in popularising ASD among low-income farmers in the tropics. Therefore, further research in search of biodegradable or durable and low-cost mulch is a must in order to popularise ASD in the tropics, especially in the developing world. However, application of ASD to the high-value crops such as strawberries and greenhouse grown tomatoes rather than the low-value crops such as spinach, banana, and eggplant may give a considerable income to the farmers. Finally, high quality research on ASD in the tropics should be extensively carried out.

Author Contributions

Conceptualization, A.K.H.P. and R.N.A.; formal analysis, A.K.H.P. and R.N.A.; writing—original draft preparation, A.K.H.P.; writing—review and editing, R.N.A. and A.K.H.P.; visualization, R.N.A.; supervision, R.N.A.; project administration, R.N.A.; funding acquisition, R.N.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by “ICGEB grant CRP/LKA18-03” and the world academy of science (TWAS) research grant number “18-020 RG/BIO/AS_I”.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data available on request.

Conflicts of Interest

The authors declare no conflict of interest.

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