Spanish Journal of Agricultural Research 15(2), e10R01, 11 pages (2017) eISSN: 2171-9292 https://doi.org/10.5424/sjar/2017152-10143 Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, O.A., M.P. (INIA) REVIEW ARTICLE OPEN ACCESS Cobweb, a serious pathology in mushroom crops: A review Jaime Carrasco1,2, María-Jesús Navarro1 and Francisco J. Gea1 1Centro de Investigación, Experimentación y Servicios del Champiñón (CIES). 16220 Quintanar del Rey, Cuenca, Spain. 2Department of Plant Scien- ces. University of Oxford. South Parks Road. Oxford, OX1 3RB, UK. Abstract Cobweb is a fungal disease of commercially cultivated mushrooms. Several members of the ascomycete genus Cladobotryum sp. have been reported as causal agents. White button mushroom is the most frequently cited host, but a wide range of cultivated edible mushrooms suffer cobweb. The pathology causes production losses and reduces the crop surface available. The parasite produces a great number of harmful conidia that can be released easily and distributed throughout the mushroom farm to generate secondary points of infection. To prevent initial outbreaks, hygiene is of primary importance within the facilities dedicated to mushroom cultivation, while additional measures must be implemented to control and reduce cobweb if there is an outbreak, including chemical and biological methods. This review summarizes and discusses the knowledge available on the historic occurrence of cobweb and its impact on commercial mushroom crops worldwide. Causal agents, disease ecology, including the primary source of infection and the dispersal of harmful conidia are also reviewed. Finally, control treatments to prevent the disease from breaking out are discussed. Additional keywords: Cladobotryum; fungal disease; dispersal; production losses; edible mushroom; control. Authors’ contributions: Conception or design; acquisition, analysis, and interpretation of data; drafting of the manuscript; and coordinating the research project: JC. Critical revision of the manuscript for important intellectual content; administrative, technical, or material support; and supervising the work: JC, MJN and FJG. Obtaining funding: FJG. Citation: Carrasco, J.; Navarro, M. J.; Gea, F. J. (2017). Cobweb, a serious pathology in mushroom crops: A review. Spanish Journal of Agricultural Research, Volume 15, Issue 2, e10R01. https://doi.org/10.5424/sjar/2017152-10143 Received: 22 Jun 2016. Accepted: 29 May 2017 Copyright © 2017 INIA. This is an open access article distributed under the terms of the Creative Commons Attribution (CC-by) Spain 3.0 License. Funding: MINECO, Spain (Project RTA2010-00011-C02) and FEDER (Project E-RTA2014-00004-C02). JC was the recipient of a fellowship from the FPI-INIA program of Ministerio de Economia y Competitividad. Competing interests: The authors have declared that no competing interests exist. Correspondence should be addressed to Jaime Carrasco: [email protected]; [email protected] Introduction cycles. First, small, white circular patches appear on the casing soil or basidiomes. These quickly spread by Many fungal diseases can affect commercial means of a fine grey-white mycelium that resembles a mushroom crops (Fletcher & Gaze, 2008). Among them spider web (Carrasco et al., 2016a). Eventually patches cobweb is considered one of the most serious diseases of mycelium start to sporulate, producing masses of dry for white button mushroom [Agaricus bisporus (Lange) spores that are easy to release when they are physically Imbach] cultures, the most widely cultivated species disturbed, mainly through watering or picking (Royse, 2014). Other edible cultivated mushrooms operations − even air currents from air-conditioning may also develop the harmful pathology (Gea et al., systems are sufficiently strong to mobilize the harmful 2011, 2017; Back et al., 2012; Kim et al., 2012). Its spores (Adie et al., 2006). Once released, conidia are occurrence in commercial crops results in reductions in spread throughout the mushrooms facilities by air yield and quality, mainly due to cap spotting, a lesser currents to form secondary colonies on the casing layer surface area that can be used for cultivation and to or to simultaneously spot the basidiomes (Adie, 2000). the need for early crop termination when the disease As soon as a primary cobweb outbreak is located over becomes epidemic (Adie, 2000; Adie et al., 2006). the casing or carpophores, it must be treated before Cobweb appears more often at the end of the sporulation, covering the infected area with thick crop cycle (although the earlier it appears, the more damp paper to avoid the release of conidia and disease devastating it can be) during the autumn and winter dispersion (Pyck & Grogan, 2015). 2 Jaime Carrasco, María-Jesús Navarro and Francisco J. Gea Various species of filamentous fungi inhabiting soil, & Savoie, 2010), Korea (Back et al., 2010), India (Bhatt decaying wood and wild-mushrooms may cause cobweb: & Singh, 2002), Ireland (McKay et al., 1999), Japan Cladobotryum dendroides (Bull.: Fr.) W. Gams & Hoozem (Sawada et al., 2005), New Zealand (De Hoog, 1978), (conidial state of Hypomyces rosellus) is the species Poland (Ślusarski et al., 2012), Serbia (Potočnik et al., historically associated with cobweb in A. bisporus crops, 2008), South Africa (Eicker, 1984), Spain (Gea et al., in recent years Cladobotryum mycophilum (Oudem.) W. 2012), Taiwan (Kirschner et al., 2007), Turkey (Bora Gams & Hoozem (conidial state of Hypomyces odoratus) & Özaktan, 2000); UK (Adie et al., 2006) and the USA has become the most commonly reported causal agent (Beyer & Kremser, 2004). (Back et al., 2012; Kim et al., 2014; Chakwiya et al., Historically treated as a minor disease, cobweb 2015; Carrasco et al., 2016a; Zuo et al., 2016). However, is currently considered one of the four most serious several other species have been reported as causing this diseases of mushroom crops caused by parasitic fungi, pathology in commercial mushroom crops. together with dry bubble (Lecanicillium fungicola), Control methods must be implemented through hygiene green mould (Trichoderma aggressivum) and wet measures and by preventing the dissemination of spores, bubble (Mycogone perniciosa) (Fletcher & Gaze, which are dry and easy to dislodge. When not properly 2008). In the mid-1990s, cobweb was reported to be the treated, conidia will spread within crops, magnifying most serious disease affecting mushroom cultivation in infection and increasing losses (Adie et al., 2006; Pyck UK and Ireland, where it reached epidemic proportions & Grogan, 2015). In this respect, public policies aimed that involved production losses of up to 40% (Adie et at reducing the use of chemical pesticides through the al., 2006). use of sustainable agriculture practices (e.g. the French The prevalence of cobweb disease in commercial “Ecophyto 2018” plan) have led to the intensification of mushroom crops has been reported to vary between 6.8 biological control efforts in agriculture. Although there and 28% in Indian A. bisporus facilities (Seth & Dar, have been attempts to identify biological control agents 1989; Bhatt & Singh, 2002), 33% in Turkey (Bora & and environmentally-friendly biomolecules that are Özaktan, 2000) and, up to 32% in Spanish commercial effective against fungal diseases in mushroom (Potočnik et button mushroom crops (Carrasco et al., 2016a). al., 2010; Kosanović et al., 2013; Gea et al., 2014; Geösel Its occurrence is associated with final flushes and is et al., 2014), no efficient bio-treatment to control cobweb conditioned by the season (McKay et al., 1999; Adie, disease has been described. In view of this, control of the 2000; Desrumeaux, 2005). The occurrence and severity pathology still relies on the use of chemical fungicides. of cobweb gradually increases from the first to the third However, since the sensitivity of mycoparasites to flush. Although it may be established at any time during approved pesticides is gradually diminishing and signals the year, it is of particular concern in autumn and winter of resistance have been detected (McKay et al., 1998; Gea (Carrasco et al., 2016a). et al., 2005; Grogan, 2006), their use demands judicious management. In short, to optimize integrated disease control, the use of chemicals must be combined with good Causal agent farming practices and with measures directed towards enhancing hygiene within growing facilities. Several species belonging to the genus Cladobotryum Nees emend. (syn. Dactylium Nees) can cause cobweb Cobweb disease: a recurrent visitor disease in edible mushroom crops (Table 1). They correspond to the conidial or asexual stage of species from the genus Hypomyces (Fries) L.R.Tulasne Cultivated edible mushrooms are susceptible to (Ascomycota, Hypocreales, Hypocreaceae). diseases caused by bacteria, fungi and viruses. Among As a rule of thumb, for its correct identification, biotic agents, mycoparasites are responsible for the Cladobotryum spp. must be evaluated by two greatest mushroom crop losses, which have a significant independent methods: (1) morphology: screening for economic impact on industry (Fletcher & Gaze, 2008). aurofusarin and camphor odour producers, registering Cobweb disease has been known as an edible conidia and phialide size as well as taxonomic characters mushroom crop pathology since the early days of (Carrasco et al., 2016a); and (2) molecular and mushroom cultivation (Carrasco, 2016). The pathology phylogenetic analysis. The best approach for complete