Diseases and pests of mushrooms in cultivation

Diseases (See chapter 16, specifically section 16.13 p. 443, of 21st Century Guidebook to Fungi)

The various diseases of mushroom crops can be caused by several fungi, bacteria or viruses. They can cause anything from slight deformities which can be unnoticed because of the variability of the crop, to damage so severe that no marketable mushrooms are produced. Therefore research to identify the pathogens responsible and develop preventative measures is of great economic significance.

In the present day a large number of fungi parasitise others of their kind and those that attack commercially grown mushrooms often cause major economic losses to the industry; so we will briefly describe some of the mycoparasites that cause disease in mushroom farms, particularly those of the most widely cultivated mushroom, Agaricus bisporus. Cultivated mushrooms are prone to bacterial and virus diseases that can cause significant crop losses, but these are outside our current area of interest. The two most common and geographically most widespread mycoparasites of A. bisporus are the Ascomycota Mycogone perniciosa (cause of the disease known as wet bubble or white mould) and Verticillium fungicola (cause of the disease known as dry bubble or brown spot).

These parasites can cause serious economic losses to the mushroom farmer, and they also cause similar diseases of the paddy straw mushroom, Volvariella volvacea, in cultivation. Vegetative mushroom mycelium is not adversely affected by Mycogone perniciosa in vitro until after formation of the strands from which the fruit bodies develop. Verticillium hyphae grow over the mushroom mycelium in vitro, eventually causing severe necrosis of the Agaricus mycelium.

Verticillium causes more mushroom necrosis than M. perniciosa and it also kills mushroom mycelium, whereas M. perniciosa does not. When M. perniciosa grows on a mushroom fruit body its growth is thick, velvety and white (which is why it is called white mould), while Verticillium produces a fine, greyish-brown felted growth (which is why it is sometimes called a cobweb mould though this is usually applied to a Cladobotryum infection; see below).

A common result of parasitism by M. perniciosa and Verticillium is a drastic effect on mushroom development, and mushroom abnormalities are the prime disease symptoms. The extent of the symptoms depends on the stage of development reached at the time of infection; the earlier the infection occurs, the greater the deformity caused. The most extreme effect is for a spheroidal mass of undifferentiated tissue to be formed rather than a mushroom; these are the ‘bubbles’ of these two bubble diseases. The undifferentiated masses caused by M. perniciosa can be 5 cm or more across, whereas those caused by Verticillium are usually less than 1 cm in diameter.

Infection with Verticillium at later stages of development causes developmental deformities, including bulbous stems with vestigial caps and fruit bodies in which the tissues are broken and peeled back. Infection of well-developed fruit bodies by M. perniciosa commonly results in abnormal enlargement of the gills (lamellae) as they become covered by the parasite. Internally, Mycogone infected mushrooms become wet and develop a foetid odour, and drops of a clear amber-coloured liquid are often extruded from the mushroom (which is why it is called wet bubble disease). Verticillium-infected sporophores are dry and shrivelled at first (dry bubble disease), but in both cases bacteria invade and a bacterial rot results. Although these mycoparasites are certainly able to produce enzymes capable of degrading mushroom hyphal wall polymers most of the rot that occurs in the final stages of these infections is due to secondary (opportunistic) invasion of the necrotic tissues by bacteria and other fungi.

Mushrooms are prone to Bacterial Blotch Disease (also known as Brown blotch or Bacterial spot) caused by the bacterium Pseudomonas fluorescens biotype G (also known as P. tolaasii). This can be endemic on mushroom farms, causing considerable crop losses by reducing yield and mushroom quality in both A. bisporus and Pleurotus (oyster mushroom). The keys to control are a dry atmosphere and basic antiseptic cleanliness. Blotch occurs when the mushroom surfaces remain wet after the compost is irrigated by misting. The bacterium grows rapidly in the fluid, causing the formation of lesions on mushroom tissue that are pale yellow to begin with, but which later become a dark brown. This discoloration is superficial, but underlying mushroom tissue may appear to be water soaked and grey or yellow-grey. Blotches often appear in the early button stage, but can appear on mushrooms of any age, and will even form on harvested  mushrooms during refrigeration or after packaging if the conditions are too moist.

The bacterial pathogen is probably present in most casing material, even after pasteurisation, but disease development is strongly influenced by environmental and surface-moisture conditions and its control requires that conditions favouring bacterial reproduction on the mushroom surface are avoided. Warm air circulated over the beds after irrigation will dry the mushrooms. Adding sodium hypochlorite at 150 ppm chlorine to the irrigation water will control blotch, but only if the mushrooms are kept dry. On wet mushrooms the bacteria can reproduce so quickly that they can neutralises the effect of the chlorine.

Virus-like particles (VLPs) have been observed in electron micrographs of many fungi. They are very similar in appearance to small spherical RNA viruses, but there is little evidence that these particles are effective in hypha-to-hypha infection. Many of the observed VLPs are presumably degenerate or defective viruses that can only be transmitted by hyphal fusions. No vectors are known for fungal viruses; transmission seems to depend on hyphal fusions. Unexpectedly, virus infections of fungi usually cause no recognizable phenotype. The exception is a mycovirus of Agaricus bisporus, which causes La France disease and ruins the crop. Diseased crops contain three virus particles and require up to ten different RNA molecules to produce infective particles; as though some are defective viruses and others are helper viruses, or perhaps different viruses perform complementary, but essential, functions.

Pests (See chapter 11, specifically section 11.2 p. 267, of 21st Century Guidebook to Fungi)

The cultivated mushroom Agaricus bisporus when grown in purpose built mushroom houses is not affected by many pests because they often do not survive the composting process. Pests often colonise a crop after this process, and the casing material can be the source of mites, nematodes and fly larvae.

Most control measures rely on insecticides which are costly and hazardous to human health and the environment. Therefore alternative measures such as integrated pest management are beginning to be used which involve introducing the pest’s natural predators to the area.
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Eelworm	Mite

The larvae (or maggots) of many small dipteran flies are probably the most frequently seen mycophagous animals; it is rare to find a mushroom in the field that is completely free of maggots. Adult females lay their eggs on the fungal fruit body and when they hatch the larva eats its way into the tissue, and subsequently eats and tunnels through the fruit body tissue, causing enormous damage. These are ‘mushroom flies’; they are about the size (one to a few millimetres long) of fruit flies (family Drosophilidae), to which they are related. Indeed there is one fruit fly, Drosophila funebris, which lays its eggs in mushroom cap tissues.

However, the specialised mushroom flies belong to the related families Sciaridae (commonly known as dark-winged fungus gnats), Phoridae (humpbacked
flies, also known as scuttle flies because of their habit of escaping by running rather than flying) and Cecidomyiidae (called cecids, are gall midges or gall gnats, the larvae of most of which feed in plant tissues, creating abnormal growths called galls).

Larvae of sciarids tend to tunnel from the bottom of the mushroom stem upwards, rarely burrowing into the cap; damage caused by phorids tends to be from the top of the mushroom downwards. Both also eat mycelium. Cecid larvae feed on mycelium and the base of primordial mushroom stems; some also have a taste for mushroom gills.

There are a few species of sciarids that are common, and one, Lycoriella solani, has become a very damaging pest of mushroom farms because it has developed resistance to organophosphorus insecticides. Adults can affect the crop by spreading mites, bacteria and spores of weed fungi around the mushroom house. Serious crop damage is caused by the larvae tunnelling through the stems of maturing mushrooms, but the most critical damage results from infestation early in crop growth because the larvae can destroy developing mushroom primordia and completely devastate the crop.

Phorid flies are common; their larvae are generally omnivorous, eating anything from decaying vegetation to fresh meat, and these flies are very diverse, the genus Megaselia alone having over 100 species in the UK. But one species, Megaselia halterata, has become an important pest of mushroom farms because the larvae eat mushroom mycelium (the female is attracted to freshly growing mycelium to lay her eggs) and the adults spread the disease-causing fungus Verticillium. Larvae of other species of Megaselia feed on and in developing mushrooms, causing tunnelling damage to mushroom cap and stem. Megaselia nigra is the species most often found causing tunnelling in wild mushrooms and can become a pest in mushroom farms.

Cecidomyiidae are so small that the adults are seldom seen, so although over 3000 species have been described there are probably more awaiting discovery. Many species are economically important as pests of crop plants. Others produce predaceous larvae that prey on other arthropods. Six species have been found on mushrooms, the most frequently encountered being Heteropeza pygmaea. An unusual feature of the cecids is that the larvae reproduce by paedogenesis, an asexual process in which a cecid larva becomes a ‘mother larva’ from which 10 to 20 daughters emerge within a week of the mother larva hatching from its egg. This method of reproduction leads to rapid multiplication which produces larval swarms capable of doing enormous damage to mycelium and mushrooms.

Mites are at least as numerous in soil as collembola and are also very small, being in the region of 250 mm long. Most are predatory, feeding on nematodes and other arthropods, but there are others that favour bacteria and fungi. Red pepper mites (Pygmephorus spp.) feed only on Ascomycota, particularly Trichoderma spp., and are often associated with composts (including mushroom farm composts) in which these moulds can be abundant. They are not primary pests of the mushroom farm but they indicate the presence of the Trichoderma weed mould, which can itself cause mushroom crop losses. The most important mite pest of mushroom farms is Tarsonemus myceliophagus; the clue is in the species name! This is a very small animal (about 180 mm long) that feeds preferentially on fungal mycelium. Because of its small size it can go unnoticed until damage symptoms appear in the mushroom crop.

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