This article was downloaded by: [KU Leuven University Library] On: 23 April 2014, At: 05:43 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK International Journal of Vegetable Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/wijv20 Mushroom Pest and Disease Management Using Plant-Derived Products in the Tropics: A Review R. T. Gahukar a a Arag Biotech Private Limited , Reshimbag , Nagpur , India Accepted author version posted online: 02 Apr 2013.Published online: 11 Nov 2013. To cite this article: R. T. Gahukar (2014) Mushroom Pest and Disease Management Using Plant-Derived Products in the Tropics: A Review, International Journal of Vegetable Science, 20:1, 78-88, DOI: 10.1080/19315260.2012.732204 To link to this article: http://dx.doi.org/10.1080/19315260.2012.732204 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the âContentâ) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms- and-conditions International Journal of Vegetable Science, 20:78â88, 2014 Copyright © Taylor & Francis Group, LLC ISSN: 1931-5260 print / 1931-5279 online DOI: 10.1080/19315260.2012.732204 Mushroom Pest and Disease Management Using Plant-Derived Products in the Tropics: A Review R. T. Gahukar Arag Biotech Private Limited, Reshimbag, Nagpur, India Mushrooms cultivated under protected culture or growing wild are infested by insects, mites, nematodes as well as bacteria and fungi. Consumers prefer mushrooms that are not treated with synthetic pesticides. Alternatively, plant-based products in various formulations have been found to be effective through different modes of action against insects and mites; that is, antifeedants, pesticides, growth regulators, repellents, and oviposition deterrents. Inhibition of spore germination and growth retardation in pathogens and arresting penetration of nematodes into stalks and sporophores are other actions. Plant-derived products can be recommended to substitute for synthetic chemicals in the commercial production of edible mushrooms. Keywords Crude plant extracts, Commercial products, Global perspective, Integrated pest management. Edible mushrooms are found in forest, fallow lands, and cultivated areas. For commercial production, mushrooms are cultivated under controlled con- ditions indoors or outside. Information on production, protection from pests and diseases, nutritional values, and economic benefits is available (Fletcher et al., 2007; Miles and Chang, 2004; Rai et al., 2007). Mushrooms have gained importance due to their medicinal properties and nearly 60% of production of medicinal species is from China (Banik, 2010). In the international market, fresh and dried mushrooms and powdered and tinned products are available. Commercial exploitation through export has been profitable for fresh mush- rooms and their by-products. Wild species are generally consumed locally by tribal people who do not adopt any control measures against pests and dis- eases. About 40% of the world production is white button mushroom, Agaricus Address correspondence to R. T. Gahukar, Arag Biotech Private Limited, Plot 220, Reshimbag, Nagpur 440009, India. E-mail:
[email protected] D ow nl oa de d by [K U Le uv en U niv ers ity L ibr ary ] a t 0 5:4 3 2 3 A pr il 2 01 4 Mushroom Pest and Disease Management 79 bisporus (Lange) Sing., followed by oyster mushrooms, Pleurotusos treatus (Jacq. Ex Fr.) Kumm., P. sajor-kaju (Zadrazil), and Pleurotus spp. (25%). The paddy straw mushroom, Volvariella volvacea (Bull ex. Fr.) Singer (16%), and a wild black forest mushroom or Shiitake, Lentinula edodes (Berk.) Pegler (19%), are available in some markets (Banik, 2010). In cultivated mushrooms, chem- icals are extensively applied to maintain room sanitation and reduce damage caused by insects and diseases. Synthetic insecticides (malathion, perme- thrin), insect growth regulators (cyromazine, diflubenzuron, methoprene), and fungicides (benomyl, chlorothalonil, thiabendazole) are regularly applied after spawning and during casing, a week later, and between flushes up to 2 days before harvesting (Anonymous, 2010). The misuse/overuse, faulty application, and persistence of chemicals may create secondary effects such as resurgence of secondary pests, pest resistance to common pesticides, environmental pollu- tion, and hazards to nontarget organisms including beneficial fauna. Further, some isolates of mildew fungus resistant to thiabendazole are also resistant to benzimidazole fungicides (Beresford, 2004). Mushrooms are fungi, and any fungicide-based control program in commercial production will affect the crop species. The norms assigned for food products by the Codex Alimentarius Commission, an agency of the Food and Agriculture Organization and the World Health Organization are often neglected in retail marketing. Similarly, stringent standards set by importing countries are not always respected in export consignment. Currently, there is increasing awareness about organic products and consumers often pay premiums for certified foods. Among pro- gressive measures, the inclusion of ecofriendly, effective, and less costly measures in mushroom protection seems to be an appropriate step. However, information on the use of plant-based products is scant and not easily avail- able. In this article, the literature on indigenous plant material for control of insects and diseases is reviewed and their use is discussed to determine the efficacy of their integration in pest and disease management and make mushroom cultivation profitable. PESTS AND DISEASES MANAGED WITH PLANT-DERIVED PRODUCTS Indigenous plants containing allelochemicals/bioactive constituents are found in the tropics but have not been exploited in preventive or curative mea- sures against pests and diseases. In general, neem (Azadirachta indica A. Juss.) has been extensively studied in agricultural crops. Neem products con- tain limonoids, terpenoids, flavonoids, and alkaloids; azadirachtin (AZ) ia a major bioactive isomer (Gahukar, 1995). These constituents may act as oviposition deterrents, sterilants, antifeedants, growth regulators, or contact toxins/poisons against insects and mites. Inhibition of spore germination and D ow nl oa de d by [K U Le uv en U niv ers ity L ibr ary ] a t 0 5:4 3 2 3 A pr il 2 01 4 80 R. T. Gahukar retardation of growth are major modes of action against pathogens. With neem products, penetration by nematodes in fruiting bodies and development of juve- niles can be restricted. It is a general practice for farmers to control pests and diseases by using crude preparations such as neem seed kernel powder, neem leaf extract, neem seed kernel extract (NSKE), neem oil, and defatted neem cake (NC). Similarly, over 50 commercial/formulated products based on neem extract in water or a chemical solvent as an emulsifiable concentrate (EC) are available in the market (Gahukar, 1998). Neem-based âready-to-useâ products are being widely used. Insects Flies, midges, beetles, and springtails are common pests that cause dam- age to cultivated mushrooms (Deepthi et al., 2003, 2004). Among flies, larvae of the phorids/humpback flies, particularlyMegaselia halterata (Wood),M. nigra Borg, andM. bovistaGimmerthal (Phoridae), feed on fungal mycelium and tun- nel into fruiting bodies. Flies damage sporophores and act as vectors of mites, nematodes, and bacterial and fungal pathogens. The infestation ofM. halterata in button mushroom can be controlled with application of neem-based products (NeemAzal, Greeneem) or hot water extract of the flowering plants Origanum onites L. or Pimpinella anisum L. (Erler et al., 2009). Larvae of sciarid flies (Sciaridae), Bradysia tritici Coq. (Sciara ocellaris Comstock), common in tropical countries, feed on compost and mycelium and occasionally burrow into fruiting bodies. Adults carry mites, nematodes, and fungal and bacterial spores. Rizwana et al. (2011) conducted an in vitro study in which NSKE (2%, v/v) completely inhibited mycelium growth in button mushroom by 72 h after application; water extract of the plantsDatura stramo- nium L., Chrysanthemum cinerariifolium (Trevir.) Vis., Juglans regia L., and Matricariach amomilla (L.) Rydb. were less effective. Rizwana et al. (2010) reported 75.9% mortality of fly larvae with an aqueous extract (20%, v/v) of neem leaves followed by C. cinerariifolium (62% mortality) and Artemisia absinthium L. (51% mortality). Two species of staphylinid beetles (Staphylinidae), Scaphisomanigro fasciatus Champion (Deepthi et al., 2003) and S. tetrastictum Champion (Mazumdar et al., 2005), feed on sporocarps, resulting in undeveloped pin- heads; adults and larvae of the cigarette beetle, Lasioderma serricorne Fb. (Dermestidae), feed on dried mushrooms (Kumar et al., 2004b). In oyster mushroom, Mazumdar et al. (2005) recorded lower larval populations of S. tetrastictum in fruit bodies after treatment with the neem product Achook EC (0.3%, v/v) containing 0.15% (w/v) AZ which was as effective as Delphin WP (0.06%, w/v) containing spores of the bacterium Bacillus thuringiensis Berl., whereas Nimbecidine EC (0.2%, v/v) containing 0.3% AZ (w/v) was less effective. On the basis of integrated management of the pest complex, Bhat D ow nl oa de d by [K U Le uv en U niv ers ity L ibr ary ] a t 0 5:4 3 2 3 A pr il 2 01 4 Mushroom Pest and Disease Management 81 et al. (1998) suggested applying endosulfan 35 EC (0.15%, v/v) at spawning and after opening of cubes because two neem-based products Neemark EC (0.03%, v/v) and Rakshak (0.03%, v/v), both containing 0.15% (w/v) AZ, could not reduce pest population and also damaged sporocarps. Mites Three mite species, Tarsonemus myceliophagus Hussey (Tarsonemidae), Tyrophagus lantneri Osb. (Phytosiidae), and Caloglyphus mycophagus (Megnin) (Acaridae) are considered economically important pests (Kumar et al., 2004a). Pest infestation takes place soon after spawning, and dam- age to fruiting bodies appears as small cavities in the stem and cap. These mycelium-eating mites feed on all parts of the mushroom, causing high yield loss. To control mites on paddy straw mushroom, Rathaiah et al. (1997) recom- mended spraying ethion 50 EC (2.5 mL·Lâ1) on paddy straw at 100 mL·kgâ1 straw. This treatment reduced pest populations up to 90% compared to appli- cation of turmeric powder (Curcuma domestica L.), NC, and a neem-based EC formulation Neemark (0.3%) with 50% mortality in A. composticola popula- tion and increased mushroom yield by 26%â33%. Similar results were reported with NC and Achook (3 mL·Lâ1; Gitanjali and Nandal, 2001). Neem products were equal in bioefficacy to diflubenzuron 20 wettable powder (WP) (0.025%, w/v) against A. composticola infesting button mushroom (Baba, 1990). Plant residues used in compost can help to reduce nematode infestation because decomposition products such as propionic acid, butyric acid, phenyl propionic acid, and other fatty acids are known to be toxic to nematodes (Tousson et al., 1968). Diseases Mushroom diseases are caused by infection by bacteria and fungi, the latter being severe on all types of mushrooms. Viral diseases are common D ow nl oa de d by [K U Le uv en U niv ers ity L ibr ary ] a t 0 5:4 3 2 3 A pr il 2 01 4 82 R. T. Gahukar in button mushroom whenever the dieback disease prevails. Aspergillus spp. attacking mushrooms during storage, particularly in humid conditions, causes rotting. Another fungus, Diehlomyces microsporus Gilke, is pathogenic to mycelium of button mushroom in the compost and produces brain-shaped fruiting bodies (False truffle/Calves brains). Various plant-based products have been used for mushroom protection. Leaves of neem and eucalyptus (Eucalyptus sp.) could be effective in controlling all pathogenic fungi in button mushroom (Sharma and Jandaik, 1994). When NC was mixed with leaves of Eichhornia crassipes (Mart.) Solms. in compost at 3 g·kgâ1 at spawning there was a decrease in mycelium growth and up to 100% control of D. microsporus, Aspergillus bitorquis (Quel.) Sacc., and A. bisporus Kwon-Chung & Funnell (Sharma, 1998). In mushrooms infected with Hypomyces rosellus (Alb. & Schwein) (anamorph Dactylium dendroides (Bull.) Fr. (Cobweb, mildew), white to pink cobweb-like puffy mold appears only on the later flushes. This cottony, wool- like mycelium sometimes turns pink or red and mushrooms turn brown and die. Complete disease control has been reported using two neem-based products (Rakshak and Neemol) applied at 0.1% (v/v) and three synthetic fungicides: Carbendazim, Sporgon containing procloraz 50 WP or Anthracol containing Propineb 70 WP, all at 0.1% (v/v) in oyster mushroom (Sharma et al., 2006). Three species of trichoderma (green molds), Trichoderma viride Pers., T. harzianum Rifai, and T. koningi Lieclaf, parasitize mushroom mycelium. As a result, dark green patches appear on casing spreading later to lesions on stems. In vitro application of water extract (5%), prepared from the leaves of neem or chrysanthemum (Chrysanthemum indicum L.); adding leaves of neem, Aegle marmelos (L.) Corr. Serr., Ricimus communis L., or Tagetes erecta L.; leaves and flowers of Eucalyptus hybrida Maiden; or leaves and rhizomes of Acorus calamus L., to compost at spawning preinoculated with Trichoderma spp. resulted in 20%â28% inhibition in growth of green mold and doubled yield of button mushroom. A water extract ofR. communis stimulated mycelial growth, which proved beneficial in mushroom production (Raina et al., 2003). The preliminary symptoms of wet bubble/white mold,Mycogone perniciosa (Magnus) Delacr., include dense white growth on gills; swollen stems and caps from which reddish-brown liquid oozes and produces a chlorine like smell; and crinkled, walnut-like bodies appear in the compost and later on the surface of the casing. In case of late infection, the leading edge becomes yellow and dies. Mishra and Singh (2003) used a water extract (5% v/v) of 24 plants, cake of neem or linseed (Linum usitatissimum L.), and reported significant reduction (up to 32%) in radial growth of mycelium with an extract of A. marmelos and Cleome viscose Linn. Further, when the A. marmelos extract was diluted with 0.5% glycerol, the inhibition rate increased to 96%. By conducting in vitro stud- ies, these authors reported significantly less incidence of wet bubble disease D ow nl oa de d by [K U Le uv en U niv ers ity L ibr ary ] a t 0 5:4 3 2 3 A pr il 2 01 4 Mushroom Pest and Disease Management 83 when a mixture of glycerol-diluted extract of A. marmelos was mixed with a fluorescent Pseudomonas sp. and Actinomycetes sp. isolate (Mishra and Singh, 2003). A few cosmopolitan fungi also attack mushrooms at various stages of fruiting development and cause economic losses. Infection of Fusarium spp. causes damping-off and withering. Infection by Verticillium fungicola var. fungicola (Preuss) Hassebr. causes dry bubble disease (brown spot) on but- ton mushroom that becomes discolored, cracked, or shriveled. At a later stage, the stem can become crooked and swollen. Brown irregular pitted areas may be seen on stems and caps, which are responsible for distortion and split- ting. Complete inhibition in growth of fungal species of six genera, Alternaria, Aspergillus, Curvularia, Fusarium, Helminthosporium, and Verticillium, was observed in vivo with 20 mL·Lâ1 of essential oil of Citrus sinensis (L.) Osbeck (Raina, 2004). In in vitro and in vivo trials conducted on paddy straw mush- room, concentrated water extract (50% v/v) of leaves of neem or tamarind (Tamarindus indica L.) mixed with water extract (1% v/v) of seeds of soap- nut tree (Sapindus trifoliatus L.) or roots of drumstick (Moringa oleifera Lam.) suppressed mycelium growth of Sclerotium rolfsii Sacc. and increased yield of saprophores (Pani and Patra, 1997). Various weed molds act as competitors for nutrients or may affect growth of mycelium by direct antagonism of mushrooms. Among them, Chaetomiumo livaceum Ames and C. globosum Kunz ex. Stand. occur if compost is of poor quality. About 10 days after spawning, grayish whitish mycelium appears and olive-green fuzz of wooly perithecia appear on the straw. Incidence of white plaster mold, Scopulariopsis fimicola (Constantin & Matrouchot), is common in wet/greasy compost on which a dense white mycelium appears. The ini- tial white mycelium of the brown plaster mold Papulaspora byssina Hotson subsequently turns into a granular cinnamon-colored mass. The occasional lip- stick mold Sporendonema purpurascens (Bonord) grows in compost and casing where it produces white mycelium, which turns bright pink and later powdery carmine red. Incorporation of dried leaves of neem, E. hybrida or R. commu- nis, at 30 g-kgâ1 of dried wheat straw in mushroom compost before spawning prevented the contamination of weed molds (Grewal and Grewal, 1998). RESEARCH AND DEVELOPMENT NEEDS Mushrooms are sold as vegetables in local markets and used fresh or pro- cessed. Therefore, use of plant-based pesticides is preferable against pests and diseases in mushroom production (Gahukar, 2007). At least eight neem-based formulations and three crude products have been studied in mushroom production. Other plants/shrubs containing alle- lochemicals found in different ecological zones are yet to be studied for isolation/extraction, synthesis and formulations, bioefficacy against pests and D ow nl oa de d by [K U Le uv en U niv ers ity L ibr ary ] a t 0 5:4 3 2 3 A pr il 2 01 4 84 R. T. Gahukar diseases, benefit of the proposed products, as well as their practicability and market potential (Gahukar, 2011). As such, the content of allelochemicals in plants differs with genetic diversity (Vir, 2007) and climatic conditions (Gupta et al., 2010), and ecotypes of neem (Senguttuvan et al., 2005) and China berry (Melia azedarach L.) (Kaul et al., 2005) with higher contents of bioactive con- stituents have been identified. In Brazil, China, India, and the United States, indigenous plants are being tested for this purpose. It will likely be neces- sary to expand the planted area of the beneficial crops to have sufficient raw materials to use for plant-based pesticides. In production rooms, black light traps (fluorescent light) can be used for monitoring phorid fly populations. Beetle populations, though remaining at low level, can be monitored in general schedules. Among mite species, Pygmephorus sp. and Histiostoma feroniarum Dufour feed on saprophagous molds and Linnopodes sp. is a voracious predator of mites and nematodes (Kumar et al., 2004a). Similarly, two fungal species, Arthrobotrys robusta Dudd and A. oligospora Fres., trap mycophagous nematodes. The potential of these beneficials should be exploited for biological control. For this pur- pose, the survival, conservation, and augmentation of predators, parasitoids, and pathogens in mushroom cultivation may be necessary to maintain their population inside rooms or outdoor cultivation areas. The feeding of larvae of fliesMycodrosophila spp. (Drosophilidae) results in a reduction in sporocarp size and often mushrooms become unfit for consump- tion. The cecidomyiid flies, Heteropeza pygmaea Winnertz, Mycophila speyeri Barnes,M. barnesiEdwards (Cecidomyiidae), whose larvae live in the compost, eat the mycelium, and ascend to the stalks and caps, are considered major pests. Similarly, bacterial spot/brown blotch is produced whenever young fruiting bodies and caps are colonized by Pseudomonas tolaasii Paine with ini- tially light brown/yellow blotches on the caps that may exude sticky residues. These pale blotches turn dark brown, covering the whole cap if mushrooms stay wet for long periods. The stem can also be affected. Another bacterium, Pseudomonas sp. (Mummy disease) infects mycelium. Fruiting bodies turn grayish, open prematurely, and the stalk becomes malformed. Subsequently, mushrooms become tough and spongy or leathery. Considering the economic importance of these pests and diseases, research needs to be initiated to evaluate plant-based products to formulate management strategies. Crude preparations (water extract) are easy to prepare with little knowl- edge and are cheaper than synthetic chemicals but have poor contact toxicity and must be ingested by pests to be effective. Plant-based products do not exhibit a knock-down effect resulting in immediate reduction in pest inci- dence. In addition, these preparations have limited shelf life because they are sensitive to high temperature, break down due to ultraviolet light, and must be applied within a few hours of preparation (Gahukar, 1998). EC-based for- mulations and ready-to-use products can be stored for at least one year and applied during any time of the day. Therefore, cheaper and locally available D ow nl oa de d by [K U Le uv en U niv ers ity L ibr ary ] a t 0 5:4 3 2 3 A pr il 2 01 4 Mushroom Pest and Disease Management 85 stickers/adhesives such as unrefined sugar, soap water, and gum arabica can be incorporated to improve residual toxicity need to be identified and their effi- cacy determined (Gahukar, 1998). In some instances, the bioefficacy of plant products is less effective than chemicals. In the future, spraying with neem oil and incorporation of neem leaves in the compost may be tried against nema- todes. In addition, many indigenous plants are found abundantly in villages but information on proper collection and storage methods is not available to growers. Growers often mix chemicals and plant products to minimize appli- cation cost. In such cases, standardization of allelochemicals and complex extracts is difficult. Similarly, process of extraction, isolation, synthesis, and formulation of plant material is time consuming and expensive (Gahukar, 2012). To ease this difficulty, new techniques can be used for accurate and rapid quantification of allelochemicals or to maintain quality norms. For example, high-performance thin-layer chromatography is a method that requires less solvent for extraction and is more efficient than other methods (Verma et al., 2011). There is always competition in the market between plant-derived prod- ucts and synthetic pesticides. Illegal use of plant products is rampant in villages in less-developed countries where legislation is not strictly executed and human poisoning may occur (Gahukar, 2012). Verification of active ingre- dients in homemade preparations poses difficulty, particularly for the mixture of extracts of different plant species. Therefore, choices should be made consid- ering safety to human health, nontarget effects including pollinators, danger to the environment, and toxicity to natural enemies (predators, parasitoids, entomopathogens). Integrated pest management (IPM) specific to edible mushrooms should include maintenance of room sanitation during production and storage, instal- lation of light traps, and frequent spraying of NSKE (5%) as prophylactic treatment. The same treatment can be repeated whenever pest attack or disease infection is noticed on mushroom beds. This condition will facilitate colonization of predatory mites. Pest economic thresholds or injury levels and disease severity grades are yet to be determined. When incidence is high, treatment with malathion 50 EC (1 mL·Lâ1) and thiabendazole 50 suspen- sion concentrate (SC) (500 mg·Lâ1) well in advance of harvest should result in pest- and disease-free stock. Appropriate IPM modules can be made available to mushroom producers for application and chemical-free production. Demonstrations and education on collection and storage of plant materials at local levels would prove beneficial as an extension activity. Local growers should be trained for mushroom cultivation using indigenous plant products and IPM. Crude preparations of plant products can be exported if facilities and avenues are available. On a global level, a network for identification of new pests and disease pathogens and monitoring of pest outbreaks and disease epidemics may be established, especially for those growers who have poor facil- ities or are using conventional methods. Spoilage of mushrooms after harvest D ow nl oa de d by [K U Le uv en U niv ers ity L ibr ary ] a t 0 5:4 3 2 3 A pr il 2 01 4 86 R. T. Gahukar and during storage is a common phenomenon due to faulty handling and unsuitable or poor storage conditions because facilities for controlled environ- ment storage are rarely or not at all available in developing and less-developed countries. These initiatives would attract producers for large-scale produc- tion even at the local level. Likewise, a gene bank of mushrooms is needed to procure authentic cultures from international collections and maintain exotic and indigenous germplasms. In the future, mushroom production units should receive more attention from food industries, export houses, and governments to form groups/associations (private, public, and nongovernmental organiza- tions) for value addition. Subsidy/initiative to producers wherever offered by government needs to be increased to motivate producers to use plant-based products. REFERENCES Anonymous. 2010. Pesticides for Agaricus mushroom production. 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