Commodity PRA for Agaricus bisporus - Defra
Commodity PRA for Agaricus bisporus - Defra
Commodity PRA for Agaricus bisporus - Defra
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A UK commodity Pest Risk Analysis <strong>for</strong> the cultivated mushroom,<br />
<strong>Agaricus</strong> <strong>bisporus</strong><br />
J.W. Woodhall 1 , J.E. Smith 2 , P.R Mills 2 & C.E. Sans<strong>for</strong>d 1<br />
1 Plant Health Group, Central Science Laboratory, <strong>Defra</strong>.<br />
2 Warwick HRI, University of Warwick.<br />
February 24 th 2009<br />
(First version: December 18 th 2007)
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
A UK commodity Pest Risk Analysis <strong>for</strong> the cultivated mushroom,<br />
<strong>Agaricus</strong> <strong>bisporus</strong><br />
Summary<br />
A commodity Pest Risk Analysis (<strong>PRA</strong>) was undertaken <strong>for</strong> the cultivated<br />
mushroom, <strong>Agaricus</strong> <strong>bisporus</strong>. The aim of the commodity <strong>PRA</strong> was to identify<br />
risks to UK mushroom crops from pathogens, weed moulds and invertebrate<br />
pests that are not present in the UK. The introduction of these organisms to<br />
UK mushroom crops has the potential to cause economic loss.<br />
The methodology <strong>for</strong> the development of the <strong>PRA</strong> was to construct lists of<br />
organisms that are potentially harmful to mushrooms, determining whether or<br />
not they are already present in the UK.<br />
The analysis determined that 19 species of fungi, 11 species of bacteria and<br />
five species of viruses were directly pathogenic to mushrooms. Weed mould<br />
fungi, whilst not directly affecting the mushroom crop, can colonise compost<br />
and cause losses through competition. This study determined that there are at<br />
least 59 species of weed mould of mushroom composts. Of the invertebrate<br />
pests associated with mushroom production, 21 insect species, 22 Acarina<br />
(mites), 28 mycophagous nematodes and at least 18 saprophytic nematodes<br />
were listed.<br />
The majority of mushroom pathogens, weed moulds and pests are present in<br />
the UK. However, one species of fungal pathogen, two species of bacterial<br />
pathogen and two species of weed mould competitor are not considered<br />
present in the UK. All known viral pathogens of mushroom are already known<br />
to occur in the UK. Of the invertebrate pests affecting mushrooms, one<br />
species of insect, seven mite species, 17 species of mycophagous<br />
nematodes and ten species of saprophytic nematodes are not present in the<br />
UK.<br />
One species that warrants further consideration with regards to the threat to<br />
UK mushroom crops is the weed mould Trichoderma aggressivum <strong>for</strong>ma<br />
aggressivum, which is present in North America. It has the potential to cause<br />
severe outbreaks of green mould if introduced to the UK. An HDC-funded<br />
Project undertook a survey of Trichoderma species present in UK mushroom<br />
production on 15 farms, over a 6-month period, commencing in December<br />
2007. Of the 28 isolates tested, T. aggressivum f. aggressivum was not found.<br />
Trichoderma aggressivum <strong>for</strong>ma europaeum is already present here (and was<br />
found in the survey). It is not known whether the North American species<br />
poses an additional risk to UK mushroom production. As Trichoderma species<br />
have the potential to spread with spawn it is feasible that this exotic species<br />
could be introduced in imported spawn. However, if sufficient inoculum was<br />
present in the spawn, then any species or <strong>for</strong>m of Trichoderma is likely to be<br />
visible and consequently the spawn would not be used. Low levels of<br />
inoculum may not be symptomatic though and could there<strong>for</strong>e escape<br />
detection. Nevertheless, testing imported spawn <strong>for</strong> the presence of non-
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
indigenous pathogens, weed moulds and pests could be useful in preventing<br />
their introduction. Testing imported spawn <strong>for</strong> indigenous organisms would<br />
also help prevent their further introduction to commercial mushroom<br />
production.<br />
Mushroom growers are advised to remain vigilant against species that are<br />
already present in the UK and have the potential to affect mushroom<br />
production, but have not yet been officially recorded in mushroom production<br />
environments. These species include several species of weed mould and<br />
nematode, and one species of fungal pathogen, Verticillium fungicola var.<br />
aleophilum. This pathogen may present a risk to UK mushrooms. It has been<br />
recorded affecting mushrooms in North America, but despite being present in<br />
other habitats in the UK, has not yet been found in UK mushroom crops.<br />
3
Contents<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
1 Introduction<br />
1.1 Mushroom production in the UK<br />
1.2 <strong>PRA</strong> initiation<br />
1.3 Aims of the <strong>PRA</strong><br />
2. Methods<br />
3. Results<br />
4. Discussion<br />
4.1 Pathogen risks<br />
4.2 Weed mould risks<br />
4.3 Invertebrate risks<br />
4.4 Conclusions<br />
5. Acknowledgements<br />
6. References<br />
Annex: List of pathogens, weed mould competitors and invertebrate pests<br />
associated with mushroom, with notes on symptoms and distribution<br />
List of Tables<br />
Table 1. Values and quantities of mushrooms home produced, imported or<br />
exported/re-exported from 1996 to 2005 with regard to the UK<br />
Table 2. UK imports of mushroom spawn (tonnes) 1996 to 2005 8<br />
Table 3. UK imports of mushroom spawn (£’000s) 1996 to 2005 9<br />
Table 4. Micro-organisms associated with mushrooms not present in the UK 12<br />
Table 5. Invertebrate pests associated with mushroom not present in the UK 13<br />
7<br />
4
1. Introduction<br />
1. 1 Mushroom production in the UK<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Mushrooms have been cultivated in the UK <strong>for</strong> at least 300 years (Flegg et al.,<br />
1985). The species of mushroom that is cultivated in the UK is predominantly<br />
<strong>Agaricus</strong> <strong>bisporus</strong>. Mushrooms are typically grown in purpose built houses or<br />
other protected environments where temperature and humidity can be<br />
controlled. However, it is reported that caves in Brad<strong>for</strong>d-on-Avon are still<br />
used <strong>for</strong> mushroom growing (Spooner & Roberts, 2005).<br />
Mushroom production is essentially in two stages, composting and mushroom<br />
growth. Composting consists of the preparation of the growth media, which<br />
usually takes 10 to 14 days. Mushroom growth typically spans 9 to 11 weeks.<br />
Mushroom farms are usually organised so that the production of a mushroom<br />
crop commences every week.<br />
Material used <strong>for</strong> preparing compost varies but usually cheap sources of<br />
carbon and nitrogen are utilised, typically wheat straw and manure. These<br />
ingredients are mixed, made into stacks and then turned and watered at<br />
intervals. The temperature can reach up to 80°C dur ing this phase (Phase I).<br />
The compost is then transferred to a pasteurisation tunnel, where the<br />
temperature is raised to 55-60°C. This is maintaine d <strong>for</strong> 6 hours then the<br />
compost is cooled and aired to remove free ammonia (Phase II). Bacteria,<br />
particularly actinomycetes and some thermpophilic fungi develop in the<br />
compost. The thermophillic organisms out-compete and effectively remove<br />
any mesophillic organisms that could infect or compete with the mushroom<br />
crop. After cooling, the media, which is selective <strong>for</strong> A. <strong>bisporus</strong>, is inoculated<br />
with spawn. Compost can be supplied to mushroom producers directly usually<br />
as Phase II or Phase III compost (described below).<br />
Spawn is a mushroom starter culture, normally grown on a cereal grain<br />
substrate. Specialist spawn producing companies, who maintain strains of A.<br />
<strong>bisporus</strong>, supply growers with packages of mushroom spawn and some<br />
compost producers provide Phase III compost (Phase II compost that is<br />
spawned and fully colonised with mushroom mycelium). This is ready <strong>for</strong><br />
casing (see below) immediately after dispatch.<br />
Spawn is mixed into the compost (0.5% by weight). The inoculated compost is<br />
then maintained at 25ºC, which is optimum <strong>for</strong> growth of mushroom mycelia.<br />
The compost is fully colonised by mycelium after 10 to 14 days and is then<br />
covered with an additional layer often including peat and chalk, to a depth of 3<br />
to 5 cm. This process is known as casing. The cased compost is then placed<br />
in the cropping room and fruiting bodies (the edible part) first appear after<br />
about two weeks. At about 7 day intervals, further flushes of fruiting bodies<br />
occur. Growers usually allow a crop to produce three flushes after which it,<br />
and the cropping house, is sterilised. The compost is then considered spent.<br />
At this stage, the cropping room is steam treated at 60ºC to kill invertebrate<br />
pests and micro-organisms and the treated spent mushroom compost is<br />
disposed of, typically <strong>for</strong> re-use by horticulturists and gardeners.<br />
5
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Like diseases of plants, diseases of mushrooms can be caused by fungi,<br />
bacteria or viruses. A variety of insect, mite and nematode pests can also<br />
affect production, directly by consuming tissue of A. <strong>bisporus</strong> (mycophagous<br />
pests) or indirectly by damaging the substrate. The presence of these<br />
organisms can cause allergies and they can be a nuisance to mushroom farm<br />
workers. Weed moulds; fungi that are capable of colonising the mushroom<br />
compost and out competing A. <strong>bisporus</strong> <strong>for</strong> available nutrients, can also cause<br />
economic loss. A severe epidemic of green mould caused by Trichoderma<br />
aggressivum f. europaeum (then classified as Trichoderma harzinum strain<br />
Th2) was first observed in Scotland and Ireland in the 1980s (Seaby, 1996).<br />
Figures on UK production, imports and exports of mushrooms between 1996<br />
and 2005 are presented in Table 1. In 2005 (latest available figures at the<br />
time of writing), the value of marketed mushrooms produced in the UK was a<br />
little over £100 million representing 74,000 tonnes. In previous years this<br />
value has been higher, with a peak (in the period covered) of £174 million<br />
representing 110,000 tonnes in 1998. The outbreak of Mushroom virus X in<br />
1998 may have contributed to the subsequent decline. This virus affected the<br />
crops of 80% of commercial mushroom growers; losses amounted to £50<br />
million, this resulted in mushroom farm closures and the loss of nearly 800<br />
jobs (NAO, 2003). UK mushroom exports peaked at 4,400 tonnes in 1997<br />
declining significantly to 100 tonnes by 2000. Thereafter exports have<br />
remained at < 300 tonnes. Since 2003, the UK has imported more<br />
mushrooms <strong>for</strong> consumption than it produces. However, the risks posed by<br />
imports of harvested mushrooms is likely to be very low. This is because<br />
home-produced mushrooms are produced in protected environments where it<br />
is unlikely that imported mushrooms would be stored.<br />
In terms of growing material, the UK mushroom industry is not self-sufficient.<br />
A significant amount of spawn (please note that the data given are <strong>for</strong> all<br />
mushroom species, not just A. <strong>bisporus</strong>) from a wide variety of countries is<br />
imported, mainly from Europe but also from North America (USA) and Asia<br />
(Tables 2 and 3). It is unlikely that the spawn from Asia is imported <strong>for</strong> A.<br />
<strong>bisporus</strong> production though. It is also not known how much spawn is imported<br />
on cereal grain and how much as phase III compost. The weight of imported<br />
spawn given in Table 2 is approximately three times more than would be<br />
needed <strong>for</strong> the quantity of mushrooms produced in the UK. There<strong>for</strong>e, phase<br />
III compost is likely to comprise a large proportion of the weight of imported<br />
spawn given in Table 2.<br />
6
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Table 1. Values and quantities of mushrooms home produced, imported or exported/re-exported from 1996 to 2005 with regard to<br />
the UK (<strong>Defra</strong>, 2006)<br />
Category<br />
1996 1997 1998 1999 2000 2001 2002 2003 2004 2005<br />
Home production marketed ('000 tonnes) 106.6 107.4 110.0 104.7 89.9 92.6 84.7 81.0 74.0 74.0<br />
Average farm-gate price (£ per tonne) 1,607.58 1,571.75 1,565.02 1,653.59 1,664.15 1,622.64 1,622.92 1,465.34 1,448.17 1,494.72<br />
Value of home production marketed (£'000) 171,295 168,741 174,456 168,559 149,545 150,298 137,448 118,693 105,518 104,092<br />
Imports quantity from all countries* ('000<br />
tonnes)<br />
51.1 86.2 68.0 59.4 68.4 72.4 75.2 99.5 110.2 134.0<br />
Imports from all countries* (£000) 84,390 139,800 109,115 99,337 108,467 118,479 125,994 152,078 159,129 173,160<br />
Exports and re-exports - quantity <strong>for</strong> the<br />
calendar year ('000 tonnes)<br />
Exports and re-exports – value <strong>for</strong> the<br />
calendar year (£’000)<br />
*Excluding the Channel Islands<br />
3.2 4.4 3.4 2.2 0.1 0.1 0.2 0.3 0.2 0.2<br />
4,196 3,060 3,711 2,549 410 367 490 550 464 433<br />
7
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Table 2. UK imports of mushroom spawn (tonnes) 1996 to 2005 from data prepared by <strong>Defra</strong> and originally sourced from HM<br />
Customs. 1<br />
Exporting country 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 Totals<br />
France 2,431.6 1,609.2 1,939.5 1,710.4 1,269.4 1,914.6 2,265.6 2,053.9 2,812.4 2,922.3 20,928.9<br />
Netherlands 821.5 753.4 833.4 1,275.6 542.8 136.4 64.2 1,463.5 835.7 922.5 7,649.1<br />
Irish Republic 176.7 82.7 39.7 117.0 371.8 650.4 1,032.6 508.8 263.7 236.5 3,479.9<br />
Italy 0.3 0.1 0.5 45.3 271.8 520.7 528.6 333.0 1,700.2<br />
USA 140.5 348.7 137.4 2.9 0.5 29.3 23.4 0.0 0.5 683.4<br />
Singapore 231.8 316.6 80.4 628.9<br />
Indonesia 158.8 146.2 305.0<br />
Germany 0.5 1.7 27.9 30.1<br />
Hungary 42.4 42.4<br />
China 0.1 0.1 40.0 40.2<br />
Belgium 0.1 0.2 0.3 5.3 7.1 13.0<br />
Denmark 1.5 6.9 4.3 1.1 0.4 0.1 14.3<br />
Japan 0.1 0.4 0.8 2.0 3.3<br />
South Africa 0.0<br />
Portugal 0.2 2.4 2.6<br />
Greece 1.5 1.5 3.0<br />
Belgium-Luxembourg 0.3 0.4 0.3 1.1<br />
South Korea 0.0 0.0<br />
Totals 3,572.4 2,803.7 2,954.7 3,149.5 2,184.6 3,138.2 4,126.6 4,654.5 4,447.0 4,494.2 35,525.4<br />
1 These figures are likely to include both cereal grain spawn and phase III compost. However, the definition used in the original data<br />
is spawn. Note: these data include figures <strong>for</strong> all edible mushroom species.<br />
8
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Table 3. UK imports of mushroom spawn (£’000s) 1996 to 2005 from data prepared by <strong>Defra</strong> and originally sourced from HM<br />
Customs 1<br />
Exporting country 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 Totals<br />
France 2,781.9 1,825.1 2,223.9 2,364.8 1,839.7 1,794.4 1,851.6 1,738.2 1,802.1 1,800.8 20,022.5<br />
Netherlands 975.5 809.5 884.8 1,317.0 549.8 64.5 39.5 575.5 244.2 362.2 5,822.5<br />
Irish Republic 242.1 137.1 65.1 37.8 385.8 748.4 1,029.8 609.9 296.3 235.8 3,788.1<br />
Italy 0.8 0.2 4.7 42.0 435.5 615.7 524.2 333.6 1,956.6<br />
U.S.A. 135.8 282.9 94.7 4.7 0.8 32.4 29.5 0.7 2.7 584.2<br />
Singapore 47.0 155.6 35.2 237.8<br />
Indonesia 45.4 85.3 130.7<br />
Germany 1.7 1.5 12.6 15.8<br />
Hungary 34.3 34.3<br />
China 0.8 0.8 5.1 6.7<br />
Belgium 0.4 1.3 1.8 8.6 13.5 25.5<br />
Denmark 3.3 14.0 8.4 1.7 1.1 0.2 28.6<br />
Japan 0.8 3.5 5.6 13.0 22.9<br />
South Africa 0.0<br />
Portugal 0.3 2.7 3.0<br />
Greece 2.4 2.2 4.6<br />
Belgium-Luxembourg 0.4 0.8 0.6 1.8<br />
South Korea 0.9 0.9<br />
Totals 4,139.7 3,074.3 3,277.5 3,760.5 2,780.3 2,743.6 3,631.7 3,612.9 2,883.0 2,783.0 32,687.6<br />
1 These figures are likely to include both cereal grain spawn and phase III compost. However, the definition used in the original data<br />
is spawn. Note: these data include figures <strong>for</strong> all edible mushroom species.<br />
9
1.2 <strong>PRA</strong> initiation<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Mushrooms could be considered to come under the EC Plant Health Directive<br />
(2000/29/EC) and subject to the same legislation as plants. However, the<br />
directive does not stipulate or exclude mushrooms specifically. In the Plant<br />
Health (England) Order 2005, the Plant Health (Northern Ireland) Order 2006,<br />
the Plant Health (Wales) Order 2006, the Plant Health (Scotland) Order 2005<br />
(hereafter collectively referred to as the Order), the term ‘plant’ includes fungi<br />
and by implication there<strong>for</strong>e includes mushrooms. This is the reason <strong>for</strong> this<br />
commodity Pest Risk Analysis.<br />
EPPO do not have any recommendations on trade in mushrooms. However,<br />
an EPPO standard exists (PP2/20) giving guidelines on good protection<br />
practices <strong>for</strong> mushrooms (Anon., 2000).<br />
1.3 Aims of the <strong>PRA</strong><br />
This <strong>PRA</strong> aims to identify the potential risks to mushroom crops from<br />
pathogens, weed moulds and pests not present in the UK. The methodology<br />
used to undertake this was to create a list of organisms associated with A.<br />
<strong>bisporus</strong>. We then went on to determine whether or not they are already<br />
present in the UK.<br />
The risks posed to the mushroom crop by organisms that are not present in<br />
the UK are discussed.<br />
11
2. Methods<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Searches of mushroom related literature (Fletcher et al., 1994; Flegg et al.,<br />
1985; Geels et al., 1988), along with host-organism indexes (CABI<br />
Compendium, undated; Farr et al., undated; Moore, 1959; Bradbury, 1986)<br />
were used to construct a list of organisms that have an association with<br />
mushrooms. Diagnosis data from samples submitted <strong>for</strong> testing at CSL were<br />
also analysed to add any recent findings of organisms associated with<br />
mushrooms to the list as these would not necessarily be published in the<br />
literature. All parts of the mushroom lifecycle were considered (spawn,<br />
mycelium and fruiting body), as well as all media associated with mushroom<br />
production (spawn, compost, harvested mushrooms).<br />
Synonyms of organisms are given as the CSL preferred name (CSL records)<br />
or <strong>for</strong> the fungal species, the name given in the Index Fungorum Database<br />
(Anon., undated). The anamorph or teleomorph of fungi is given dependent<br />
upon which stage is usually associated with mushrooms. Once the pest list<br />
was created, worldwide distribution and presence or absence in the UK was<br />
determined <strong>for</strong> each species. This was done by consulting specific literature,<br />
the CABI Compendium (CABI Compendium, undated) and CSL internal<br />
diagnosis records as well as consulting the relevant CSL or Warwick HRI<br />
specialists. For fungal species, the British Mycological Database (BMS,<br />
undated) and Farr et al. (undated) were also used. Mushroom pathogens,<br />
weed moulds and pests that are not present in the UK and which could pose a<br />
risk to mushroom production were then identified and discussed.<br />
12
3. Results<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
All organisms associated with mushroom found in the literature are listed in<br />
the tables in the Annex along with the supporting references. This analysis<br />
found that 19 species of fungal pathogens, 11 species of bacteria and five<br />
species of virus are associated with mushrooms worldwide. There are also at<br />
least 59 species of weed mould that could affect mushroom production. For<br />
the invertebrate pests, 21 insect species, 22 Acarina (mites), 28<br />
mycophagous nematodes and at least 18 saprophytic nematodes were found<br />
associated with mushroom production.<br />
Micro-organisms (pathogens and weed moulds) associated with mushroom<br />
production that are not present in the UK are shown in Table 4. Two species<br />
of weed mould competitors are not present in the UK. One fungal pathogen<br />
and two bacterial pathogens of mushroom are also exotic to the UK. All known<br />
mushroom viruses are already considered present in the UK.<br />
Table 4. Micro-organisms associated with mushrooms not present in the UK<br />
Species Type of<br />
organism<br />
Paecilomyces Fungal<br />
penicillatus pathogen<br />
Pseudomonas<br />
costantinii<br />
Pseudomonas<br />
‘reactans’<br />
Trichoderma<br />
aggressivum f.<br />
aggressivum<br />
Trichoderma<br />
asperellum<br />
Bacterial<br />
pathogen<br />
Bacterial<br />
pathogen<br />
Weed mould<br />
competitor<br />
Weed mould<br />
competitor<br />
Worldwide distribution Means of movement<br />
Only one record of<br />
isolation from a<br />
decaying mushroom in<br />
Belgium. Has also been<br />
found on decaying<br />
plants and wood.<br />
Originally found in<br />
Finland but the present<br />
distribution is unknown.<br />
Originally considered a<br />
strain of Pseudomonas<br />
tolaasii.<br />
P. ‘reactans’ strains<br />
pathogenic to mushroom<br />
were originally reported<br />
in the USA<br />
Present in North<br />
America and relatively<br />
common as a cause of<br />
green mould in<br />
mushroom compost.<br />
Recorded in mushroom<br />
compost in Hungary.<br />
Appears to have a wide<br />
global distribution. Used<br />
as a biocontrol agent<br />
against plant pathogenic<br />
fungi.<br />
Airborne spores.<br />
Direct contact,<br />
contaminated compost or<br />
introduced to the growing<br />
environment via air<br />
currents.<br />
Direct contact,<br />
contaminated compost or<br />
introduced to the growing<br />
environment via air<br />
currents.<br />
Spores spread by pepper<br />
mites (Pygmephorus spp.)<br />
Some Trichoderma species<br />
can contaminate spawn.<br />
Spores spread by pepper<br />
mites (Pygmephorus spp.)<br />
Some Trichoderma species<br />
can contaminate spawn.<br />
13
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Invertebrate pests of mushroom that are not present in the UK are listed in<br />
Table 5. These consist of one species of insect, seven mite species, 17<br />
species of mycophagous nematodes and ten species of saprophytic<br />
nematodes.<br />
Table 5. Invertebrate pests associated with mushroom not present in the UK<br />
Species Type of<br />
Worldwide Means of movement<br />
organism distribution<br />
Bradysia<br />
matogrossensis<br />
Insect (sciarid) Brazil Compost and airborne<br />
Brennandania lambi<br />
Krczal<br />
(Australian<br />
mushroom pygmy<br />
mite)<br />
Digamasellus fallax<br />
Leitner<br />
Dolichocybe keiferi<br />
Krantz<br />
Pediculaster<br />
fletchmanni Wicht<br />
Pygmephorus<br />
athiasae Wicht<br />
(Red pepper mite)<br />
Pygmephorus<br />
kneeboni Wicht<br />
(Red pepper mite)<br />
Pygmephorus<br />
murphyi Smiley<br />
(Red pepper mite)<br />
Aphelenchoides<br />
agarici<br />
Aphelenchoides<br />
asterocaudatus<br />
Aphelenchoides<br />
bicaudatus<br />
Aphelenchoides<br />
coffeae<br />
Aphelenchoides<br />
cyrtus<br />
Aphelenchoides<br />
helophilus<br />
Aphelenchoides<br />
limberi<br />
Acarina (mite) Australia Primarily through infested<br />
spawn<br />
Acarina (mite) Worldwide (not<br />
UK)<br />
Acarina (mite) USA Not known<br />
In compost or phoretic (carried<br />
by other invertebrates)<br />
Acarina (mite) Brazil In compost or phoretic (carried<br />
by other invertebrates)<br />
Acarina (mite) France<br />
In compost or phoretic (carried<br />
by other invertebrates)<br />
Acarina (mite) USA In compost or phoretic (carried<br />
by other invertebrates)<br />
Acarina (mite) USA In compost or phoretic (carried<br />
by other invertebrates)<br />
Mycophagous<br />
nematode<br />
Mycophagous<br />
nematode<br />
Mycophagous<br />
nematode<br />
Mycophagous<br />
nematode<br />
Mycophagous<br />
nematode<br />
Mycophagous<br />
nematode<br />
Mycophagous<br />
nematode<br />
India In compost or phoretic (carried<br />
by other invertebrates)<br />
India In compost or phoretic (carried<br />
by other invertebrates)<br />
Australia,<br />
Europe<br />
In compost or phoretic (carried<br />
by other invertebrates)<br />
Australia In compost or phoretic (carried<br />
by other invertebrates)<br />
Germany In compost or phoretic (carried<br />
by other invertebrates)<br />
Europe In compost or phoretic (carried<br />
by other invertebrates)<br />
Europe, North<br />
America, Asia<br />
In compost or phoretic (carried<br />
by other invertebrates)<br />
14
Species Type of<br />
organism<br />
Aphelenchoides Mycophagous<br />
minor<br />
nematode<br />
Aphelenchoides<br />
myceliophagus<br />
Aphelenchoides<br />
neocomposticola<br />
Aphelenchoides<br />
sacchari<br />
Aphelenchoides<br />
spinosus<br />
Aphelenchoides<br />
swarupi<br />
Mycophagous<br />
nematode<br />
Mycophagous<br />
nematode<br />
Mycophagous<br />
nematode<br />
Mycophagous<br />
nematode<br />
Mycophagous<br />
nematode<br />
Ditylenchus filimus Mycophagous<br />
nematode<br />
Ditylenchus<br />
intermedius<br />
Mycophagous<br />
nematode<br />
Ditylenchus valveus Mycophagous<br />
nematode<br />
Filenchus misellus<br />
Acrobeloides<br />
apiculatus<br />
Acrobeloides<br />
buetschlii<br />
Pelodera<br />
(Cylindridera)<br />
icosiensis<br />
Pelodera<br />
lambdiensis<br />
Mycophagous<br />
nematode<br />
Saprophytic<br />
nematode<br />
Saprophytic<br />
nematode<br />
Saprophytic<br />
nematode<br />
Saprophytic<br />
nematode<br />
Prodontorhaditis sp. Saprophytic<br />
nematode<br />
Rhabditis<br />
(Cephaloboides)<br />
oxycera<br />
Saprophytic<br />
nematode<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Worldwide Means of movement<br />
distribution<br />
India In compost or phoretic (carried<br />
by other invertebrates)<br />
India In compost or phoretic (carried<br />
by other invertebrates)<br />
India In compost or phoretic (carried<br />
by other invertebrates)<br />
Europe, India In compost or phoretic (carried<br />
by other invertebrates)<br />
Germany,<br />
Australia<br />
In compost or phoretic (carried<br />
by other invertebrates)<br />
India, Italy In compost or phoretic (carried<br />
by other invertebrates)<br />
Canada In compost or phoretic (carried<br />
by other invertebrates)<br />
Europe, North<br />
America<br />
North America,<br />
Asia<br />
In compost or phoretic (carried<br />
by other invertebrates)<br />
In compost or phoretic (carried<br />
by other invertebrates)<br />
Asia Not known – only observed to<br />
eat mushroom mycelia<br />
experimentally. But means of<br />
movement likely to be similar to<br />
Worldwide (not<br />
UK)<br />
Worldwide (not<br />
UK)<br />
other nematodes.<br />
Passive dispersal, survival in<br />
compost or phoretic on flies.<br />
Possibly distributed by air<br />
currents when in a dried state.<br />
Passive dispersal, survival in<br />
compost or phoretic on flies.<br />
Possibly distributed by air<br />
currents when in a dried state.<br />
China Passive dispersal, survival in<br />
compost or phoretic on flies.<br />
Possibly distributed by air<br />
currents when in a dried state.<br />
USA,<br />
Australia, Fiji<br />
and North<br />
Africa<br />
Passive dispersal, survival in<br />
compost or phoretic on flies.<br />
Possibly distributed by air<br />
currents when in a dried state.<br />
China Passive dispersal, survival in<br />
compost or phoretic on flies.<br />
Possibly distributed by air<br />
currents when in a dried state.<br />
Not known Passive dispersal, survival in<br />
compost or phoretic on flies.<br />
Possibly distributed by air<br />
currents when in a dried state.<br />
15
Species Type of<br />
organism<br />
Rhabditis<br />
Saprophytic<br />
(Choriorhabditis) nematode<br />
longicaudatus<br />
Rhabditis (Pellioditis)<br />
pellio<br />
Saprophytic<br />
nematode<br />
Rhabditis terricola Saprophytic<br />
nematode<br />
Rhabditis cucumeris Saprophytic<br />
nematode<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Worldwide<br />
distribution<br />
Means of movement<br />
Not known Passive dispersal, survival in<br />
compost or phoretic on flies.<br />
Possibly distributed by air<br />
currents when in a dried state.<br />
Worldwide (not<br />
UK)<br />
Passive dispersal, survival in<br />
compost or phoretic on flies.<br />
Possibly distributed by air<br />
currents when in a dried state.<br />
Not known Passive dispersal, survival in<br />
compost or phoretic on flies.<br />
Possibly distributed by air<br />
currents when in a dried state.<br />
Worldwide(not<br />
UK)<br />
Passive dispersal, survival in<br />
compost or phoretic on flies.<br />
Possibly distributed by air<br />
currents when in a dried state.<br />
16
4. Discussion<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
This analysis has shown that the majority of the mushroom pathogens, weed<br />
moulds and pests recorded in the literature are present in the UK.<br />
Nevertheless, several species are not found in the UK that could potentially<br />
affect mushroom production if introduced. They are discussed in part below.<br />
There are also a number species that have been recorded in other habitats or<br />
on other hosts in the UK but have not recorded in UK mushroom crops. These<br />
species include several species of weed mould and nematode, and one<br />
species of fungal pathogen, Verticillium fungicola var. aleophilum. Of these<br />
species, the most significant threat is the fungal pathogen. This organism has<br />
been recorded affecting mushrooms in North America, where it is the main<br />
cause of dry bubble disease, causing a variety of symptoms on mushroom<br />
caps such as lesions, distortion and discolouration. However, in Europe, dry<br />
bubble is associated with Verticillium fungicola var. fungicola, there<strong>for</strong>e<br />
mushroom growers already deal with dry bubble caused by a related species.<br />
Nevertheless, mushroom growers are advised to remain vigilant against<br />
species that are already present in the UK and have the potential to affect<br />
mushroom production, but have not yet been officially recorded in mushroom<br />
production environments.<br />
4.1 Pathogen risks<br />
Paecilomyces penicillatus. This fungus has not been recorded in the UK.<br />
There is only one report of it affecting mushrooms (found on a decaying<br />
mushroom in Belgium). As this was an isolated report it may have been an<br />
opportunistic infection. If P. penicillatus were an aggressive pathogen of<br />
mushrooms then it is likely that the disease would have been more widely<br />
reported. There<strong>for</strong>e the risk this pathogen presents to UK mushrooms is likely<br />
to be low.<br />
Pseudomonas species. Pseudomonas costantinii and Pseudomonas<br />
‘reactans’ have never been recorded in the UK. However, little is known about<br />
their current distribution. Pseudomonas costantinii was originally considered a<br />
strain of Pseudomonas tolaasi (Munsch et al., 2002). Both P. tolaasi and P.<br />
costantinii can cause brown blotches on mushroom caps. P. tolaasi is known<br />
to be common in the UK on mushrooms. Since many Pseudomonas strains<br />
already occur in UK mushrooms, many uncharacterised, it is possible that<br />
these species are also present but have not been <strong>for</strong>mally reported. UK<br />
mushroom growers already manage diseases caused by several other<br />
Pseudomonas species. There<strong>for</strong>e, it is likely that these Pseudomonas species<br />
present little additional risk to UK mushrooms.<br />
4.2 Weed mould competitor risks<br />
Trichoderma aggressivum <strong>for</strong>ma aggressivum. This species is an<br />
aggressive coloniser of mushroom composts in North America but is not<br />
present in Europe. An HDC-funded Project undertook a survey of<br />
Trichoderma species present in UK mushroom production on 15 farms, over a<br />
17
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
6-month period, commencing in December 2007. Of the 28 isolates tested, T.<br />
aggressivum f. aggressivum was not found (Lane, 2008). Severe outbreaks of<br />
green mould in Europe are usually associated with Trichoderma aggressivum<br />
<strong>for</strong>ma europaeum. In the UK and Ireland, T. aggressivum f. europaeum has<br />
caused severe outbreaks and economic losses (Seaby, 1996). Trichoderma<br />
aggressivum f. europaeum differs to T. aggressivum f. aggressivum by a<br />
subtly different growth rate at 25ºC and micromorphological differences<br />
(Samuels et al., 2002). Appropriate molecular tests can be used to distinguish<br />
between the two <strong>for</strong>ms.<br />
The introduction of the North American strain would increase the genetic<br />
diversity of the T. aggressivum species complex in Europe, which could<br />
present new, un<strong>for</strong>eseen, problems to European mushroom growers. There is<br />
a pathway <strong>for</strong> this species to enter the UK, as Trichoderma species can be<br />
spread with spawn, which is imported from North America (Table 2). However,<br />
T. aggressivum has not been known to infect mushrooms through spawn but<br />
has the potential to do so. It is likely that either <strong>for</strong>m of Trichoderma in spawn<br />
would be highly visible if a sufficient amount of inoculum was present and in<br />
these circumstances it would be rejected.<br />
Trichoderma asperellum. Although this species is recorded in mushroom<br />
composts in Hungary, it is not likely to present major problems to mushroom<br />
growers in the UK. This is because UK mushroom growers are used to<br />
managing more aggressive Trichoderma species, such as Trichoderma<br />
aggressivum f. europaeum. Trichoderma asperellum is present worldwide. It<br />
is used as a biocontrol agent against fungal plant pathogens in several<br />
countries. The relatively few reports <strong>for</strong> it indicate that it is likely to be one of<br />
the less aggressive Trichoderma species that can colonise mushroom<br />
composts.<br />
4.3 Invertebrate risks<br />
Bradysia matogrossensis. This species of sciarid is present in Brazil. Many<br />
Bradysia species are already present in the UK but they are rarely recorded<br />
as pests on mushroom crops. Should B. matogrossensis be introduced, it<br />
would seem unlikely to cause any additional problems <strong>for</strong> mushroom growers,<br />
who already deal with the native Bradysia species. At the present time the<br />
introduction of this species is unlikely, as there is no trade in spawn with<br />
South America (Table 2) and spawn is not a known source of infestation <strong>for</strong><br />
this species.<br />
Acarina (Mites). Mites are almost ubiquitous in mushroom production, and<br />
since they are very small they are not usually noticed until large numbers are<br />
present (Flegg et al., 1988). Several of the mite species recorded in<br />
association with mushrooms as both pests and ‘incidentals’ are absent from<br />
the UK. Should they be introduced, it is unlikely that they will pose a<br />
significant additional risk to UK mushroom growers, who already deal with<br />
several species of mites. Two of the most important species, Brennandania<br />
18
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
lambi and Dolichocybe keiferi, are absent from the UK, and these directly<br />
affect mushroom mycelia. Brennandania lambi has only ever been reported in<br />
Australia but as there is no trade in spawn from this country, there is no<br />
obvious pathway <strong>for</strong> its introduction to the UK. Conversely, D. keiferi, a<br />
species present in the USA, may have a pathway <strong>for</strong> its introduction as spawn<br />
is imported to the UK from the USA. It is likely that these species will present<br />
no new risk to UK growers who already deal with several mycophagous mite<br />
species that are common in the UK.<br />
Pediculaster fletchmanni and several ‘red pepper mites’ (Pygmephorus<br />
species) are exotic to the UK and can occur in mushroom crops. Although<br />
harmless to the mushroom crop itself (feeding mainly on weed moulds such<br />
as Trichoderma), they can, when present in large numbers, lead to crop<br />
rejection due to contamination with their brightly coloured bodies. In addition,<br />
contact with these mites can induce allergic responses in mushroom pickers.<br />
Several Pygmephorus species are already present in the UK and similar<br />
problems already occur. Should these exotic species be introduced, they are<br />
unlikely to present a new risk to UK mushroom growers and are only likely to<br />
present a problem if high levels of weed mould such as Trichoderma are<br />
present.<br />
Nematode species. Thirteen Aphelenchoides and three Ditylenchus species<br />
affect mushroom crops and are considered absent from the UK. These are<br />
mycophagous and could there<strong>for</strong>e affect mushroom yield and quality.<br />
However, Aphelenchoides composticola and Ditylenchus myceliophagus are<br />
the most important species of each genus with regards to mushroom<br />
production. These are both present in the UK but are relatively rare in UK<br />
mushroom crops. It is unlikely that other members of each species would<br />
pose more of a risk to UK mushroom crops, since UK mushroom farmers<br />
already manage the most aggressive species of each genus.<br />
Filenchus misellus is also absent from the UK. It is present in Asia and it has<br />
been observed to consume mushroom mycelia under experimental conditions.<br />
The feeding habits of this species are not fully known but they have been<br />
observed to consume other species of fungi in experiments (Okada et al.,<br />
2005). There are no further reports of the nematode in mushrooms. There<strong>for</strong>e,<br />
it appears that this species is not established in mushroom production<br />
systems. Consequently, it is unlikely that there is a pathway <strong>for</strong> this species to<br />
be introduced to UK mushrooms at this time.<br />
Ten species of saprophytic nematodes associated with mushrooms are<br />
absent from the UK. These include species of Acrobeloides, Pelodera and<br />
Rhabditis and one species of Prodontorhaditis. Several saprophytic species<br />
are common in UK mushroom production. These do not directly affect the<br />
mushroom itself, so it is unlikely that these would present a new risk to UK<br />
mushroom producers.<br />
4.4 Conclusions<br />
19
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Many of the major pathogen, weed mould and pest species of mushroom are<br />
already present in the UK. However, there is a considerable number of<br />
pathogen, weed mould and pest species of mushroom that are not present in<br />
the UK. This analysis considers that these species do not pose new risks <strong>for</strong><br />
UK mushroom growers, as they already manage similar risks presented by<br />
existing related organisms. However, T. aggressivum f. aggressivum, the<br />
main cause of green mould in North America, may still pose a threat<br />
From this analysis, testing imported spawn may be useful in preventing the<br />
movement of harmful organisms be they indigenous or non-indigenous. There<br />
has been some movement of harmful organisms in mushroom production<br />
recently, such as the movement of Trichoderma species into central Europe<br />
(Hatvani et al., 2007) and the recent movement of V. fungicola var. fungicola<br />
from Europe into North America (Largeteau et al., 2004). Testing of spawn<br />
imports, at least those from non-Member States could be considered, in order<br />
to minimise the risk from new exotic pathogens, weed moulds and pests of<br />
mushroom. An EPPO protocol <strong>for</strong> testing spawn imported into the EPPO<br />
region could also be produced.<br />
This analysis has also highlighted that there are several species that are<br />
already present in the UK and have the potential to affect mushroom crops,<br />
but have not yet been observed affecting mushroom production to date.<br />
Verticillium fungicola var. aleophilum is one such species. Mushroom growers<br />
should remain vigilant against such organisms.<br />
5. Acknowledgments<br />
The authors would like to thank CSL specialists <strong>for</strong> their input into <strong>for</strong>ming the<br />
pest lists: J. Ostojia-Starzewski (mites), D. Collins (insects), T. Prior and R.<br />
Lawson (nematodes). C. Lane is thanked <strong>for</strong> general help and advice.<br />
20
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<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
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Coles PS, 2002. Nematodes Chapter in Mushroom Integrated Pest<br />
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Collopy PD, Largeteau-Mamoun ML, Romaine CP, Royse DJ, 2001.<br />
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Grewal PS, Richardson PN, 1990. Caenorhabditis elegans (Nematoda:<br />
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Grewal PS, Siddiqi MR, Atkey PT, 1992. Aphelenchoides richardsoni sp. nov.<br />
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22
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obscura sp. nov. from India (Nematoda: Aphelenchina). Afro-Asian Journal of<br />
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Gurney B, Hussey NW, 1967 Pygmephorus species (Acarina; Pyemotidae)<br />
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Nagy A, Nagy E, Vágvölgyi C, Kredics L, 2007. Green mould diseases of<br />
<strong>Agaricus</strong> and Pleurotus species are caused by related but phylogenetically<br />
different Trichoderma species. Phytopathology 97, 532-537.<br />
Hodda M, 2003. A Checklist of Aphelenchida.<br />
[http://www.ento.csiro.au/science/nematodes/checklist_dec2003.rtf].<br />
Hooper D, 1962. Effects of a nematode on the growth of mushroom mycelium.<br />
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Hussey NW, 1963. A new species of Tarsonemus (Acarina: Tarsonemidae)<br />
from cultivated mushrooms. Acarologia 5, 540-544.<br />
Inglis PW, Peberdy JF, 1996. Isolation of Ewingella americana from the<br />
cultivated mushroom, <strong>Agaricus</strong> <strong>bisporus</strong>. Current Microbiology 33, 334-337.<br />
Jin Q, Cai W, Feng W, Shi L, Li F, 2006. Nematode species associated with<br />
the button mushroom in Zhejiang province. Acta Agriculturae Zhejiangensiss<br />
18, 195-197.<br />
Lane C, 2008. Trichoderma green mould – determining diversity and<br />
highlighting risks. HDC Project Report M46. 17pp.<br />
Largeteau ML, Mata G, Savoie J-M, 2004. Verticillium fungicola var. fungicola<br />
affects <strong>Agaricus</strong> <strong>bisporus</strong> cultivation in Mexico. FEMS Microbiology Letters<br />
236, 191-196.<br />
Liang T, Xiu O, Chongti T 1983. Studies on the plant nematodes in South<br />
Fujian III, Observation on Mushrooms-Nematodes. Acta Zoologia 29, 170-<br />
179.<br />
Lincoln SP, Fermor TR, 1999. Janthinobacterium agaricidamnosum sp. nov.,<br />
a soft rot pathogen of <strong>Agaricus</strong> <strong>bisporus</strong>. International Journal of Systematic<br />
Bacteriology 49, 1577-1589.<br />
Luangsa-ard JJ, Hywel-Jones NL and Samson RA (2004) The polyphyletic<br />
nature of Paecilomyces sensu lato based on 18S-generated rDNA phylogeny.<br />
Mycologia 96, 773-780.<br />
23
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Menzel F, Smith JE, Colauto NB, 2003. Bradysia dif<strong>for</strong>mis Frey and Bradysia<br />
ocellaris (Comstock): Two additional neotropical species of black fungus gnats<br />
(Diptera : Sciaridae) of economic importance: A redescription and review.<br />
Annals of the Entomological Society of America 96, 448-457.<br />
Miyairi K, Konno K, Harada Y, Okuno T, 1994. Fungus fruit body lytic enzyme<br />
from a myxomycete Badhamia utricularis. Mycoscience 35, 695-699.<br />
Moore WC, 1959. British Parasitic Fungi. Cambridge University Press.<br />
Munsch P, Alatossava T, Marttinen N, Meyer JM, Christen R, Gardan L, 2002.<br />
Pseudomonas costantinii sp. nov., another causal agent of brown blotch<br />
disease, isolated from cultivated mushroom sporophores in Finland.<br />
International Journal of Systematic and Evolutionary Microbiology 52, 1973-<br />
1983.<br />
NAO, 2003. Protecting England and Wales from plant pests and diseases.<br />
Report by the comptroller and auditor general. HC 1186 Session 2002-2003:<br />
29 October 2003. [http://www.nao.org.uk/publications/nao_reports/02-<br />
03/02031186.pdf]<br />
Okada H, Kadota I, 2002. Population growth rates of two fungal-feeding<br />
nematodes, Filenchus misellus (Tylenchidae) and Aphelenchus avenae<br />
(Aphelenchidae), on ten fungal isolates. Fourth International Congress of<br />
Nematology Programme and Abstracts. 8–13 June 2002, Tenbel, La Galletas,<br />
Arona, Tenerife, Canary Islands, Spain.<br />
Okada H, Harada H, Kadota I, 2005. Fungal-feeding habits of six nematode<br />
isolates in the genus Filenchus. Soil Biology and Biochemistry 37, 1113-1120.<br />
Pantou MP, Strunnikova OK, Shakhnazarova VY, Vishnevskaya NA,<br />
Papalouka VG, Typas MA, 2005. Molecular and immunochemical phylogeny<br />
of Verticillium species. Mycological Research 109, 889-902.<br />
Perkins DD, Davis RH, 2000. Evidence <strong>for</strong> safety of Neurospora species <strong>for</strong><br />
academic and commercial uses. Applied and Environmental Microbiology 66,<br />
5107–5109.<br />
Perper T, Petriello R, 1977. Population growth patterns of four species of<br />
Aphelenchoides on fungi, Journal of Nematology 9, 301-307.<br />
Phillips R, 2006. Mushrooms. Macmillan: London.<br />
Reyes JE, Venturini ME, Oria R, Blanco D, 2004. Prevalence of Ewingella<br />
americana in retail fresh cultivated mushrooms (<strong>Agaricus</strong> <strong>bisporus</strong>, Lentinula<br />
edodes and Pleurotus ostreatus) in Zaragoza (Spain). FEMS Microbiology<br />
Ecology 47, 291–296.<br />
Richardson PN, Grewal PS, 1993. Nematode Pests of Glasshouse Crops and<br />
Mushrooms. Chapter in Plant parasitic Nematodes in Temperate Agriculture.<br />
24
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Evans K, Trudgill DL, Webster JM (eds). CABI International: Walling<strong>for</strong>d. pp.<br />
501-544.<br />
Samuels GJ, 2006.Trichoderma: Systematics, the Sexual State, and Ecology.<br />
Phytopathology 96,195-200.<br />
Samuels, GJ, Dodd SL, Gams W, Castlebury LA, Petrini O, 2002.<br />
Trichoderma species associated with the green mould epidemic of<br />
commercially grown <strong>Agaricus</strong> <strong>bisporus</strong>. Mycologia 94, 146-170.<br />
Schroers HJ, Samuels GJ, Seifert KA, Gams W, 1999. Classification of the<br />
mycoparasite Gliocladium roseum in Clonostachys as C. rosea, its<br />
relationship to Bionectria ochroleuca, and notes on other Gliocladium-like<br />
fungi. Mycologia 91, 365-385.<br />
Seaby DA, 1996. Differentiation of Trichoderma taxa associated with<br />
mushroom production. Plant Pathology 45, 905-912.<br />
Sharma NK, Thapa CD, Nath A, 1981. Pathogenicity and identity of<br />
myceliophagus nematode infesting <strong>Agaricus</strong> <strong>bisporus</strong> in Himachal Pradesh<br />
(India). Indian Journal of Nematology 11, 230-231.<br />
Singh SK, Sharma VP, Sharma SR, Kumar S, Tiwari M, 2006. Molecular<br />
characterisation of Trichoderma taxa causing green mould disease in edible<br />
mushrooms. Current Science 90, 427-431.<br />
Spooner B, Roberts P, 2005. Fungi (Collins New Naturalist). London: Collins.<br />
Smilley RL, 1978. Taxonomic studies of Pygmephorus species from the<br />
western hemisphere, with a key to females and an overview of the current<br />
problems <strong>for</strong> classification (Acari: Pymotidae and Pygmephoridae)<br />
International Journal of Acarology 4, 125- 160.<br />
Steiner G, 1933. Rhabditis lambdiensis, a nematode possibly acting as a<br />
disease agent in mushroom beds. Journal of Agricultural Research 46, 427-<br />
438.<br />
Vakili NG,1989. Gonatobotrys simplex and its teleomorph Melanospora<br />
damnosa. Mycological Research 93, 67-74.<br />
van Greuning M, Eicker A, 1991. The identity of the lipstick mould of cultivated<br />
mushrooms <strong>Agaricus</strong> <strong>bisporus</strong>. Botanical Bulletin of Academia Sinica 32, 57-<br />
62.<br />
Wells JM, Saper GM, Fett WF, Butterfield JE, Jones JB, Bouzar H, Miller FC,<br />
1996. Post harvest discolouration of the cultivated mushroom <strong>Agaricus</strong><br />
<strong>bisporus</strong> caused by Pseudomonas tolaasii, P. ‘reactans’, and P. ‘gingeri’.<br />
Phytopathology 86, 1098-1104.<br />
25
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
White PF Smith JE, 2000. Bradysia lutaria (Winn.) (Dipt., Sciaridae) - a recent<br />
addition to the British fauna and a pest of the cultivated mushroom (<strong>Agaricus</strong><br />
<strong>bisporus</strong>). Entomologist’s Monthly Magazine. 136, 165-167.<br />
Wicht MC, 1970. Three new species of Pyemotid mites associated with<br />
commercial mushrooms. Acarologia 12, 262-268.<br />
Wood FC, 1957. Heleococcum aurantiacum; an uncommon weed fungus of<br />
mushroom compost. Nature 180, 283.<br />
Zamani AA, Talebi AA, Mohamedi E, 2005. Investigation on morphological<br />
and biological characteristics of Megaselia scalaris (Dipt. Phoridae) as an<br />
important pest of button mushrooms in Karaj, Iran. The Scientific Journal of<br />
Agriculture 27, 47-58.<br />
Zare R, Gams W, 2003. Lecanicillium psalliotae. IMI descriptions of Fungi<br />
1568.<br />
26
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Annex. List of pathogens, weed mould competitors and invertebrate pests associated with mushroom, with notes on symptoms and distribution<br />
Table 1. Fungal pathogens associated with <strong>Agaricus</strong> <strong>bisporus</strong><br />
Pathogen Synonyms Symptom Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Acremonium Cephalosporium Moore (1959) reported Present on a wide Present on a wide range of Flegg et al. (1985); BMS<br />
strictum<br />
acremonium that one species of range of hosts and hosts and habitats in the UK but (undated); Moore (1959)<br />
Acremonium caused habitats worldwide. no records found after Moore<br />
chocolate brown Appears to be (1959).<br />
patches on mushroom.<br />
However, the species<br />
was not identified. Flegg<br />
et al. (1985) report that<br />
A. strictum has an<br />
association with<br />
mushroom but no other<br />
reports are available<br />
that describe the<br />
interaction.<br />
cosmopolitan.<br />
Aphanocladium Acremonium album, Circular brown spots on Cosmopolitan, Present and occasionally Fletcher et al. (1994);<br />
album<br />
Nectriopsis<br />
cap, white aerial recorded on a wide causes serious outbreaks in BMS (undated)<br />
sporangiicola hyphae.<br />
range of hosts and<br />
habitats.<br />
mushrooms.<br />
Badhamia<br />
This slime mould is Cosmopolitan, Present in the UK on a wide Moore (1959)<br />
utricularis<br />
capable of attacking the recorded on a wide range of hosts and habitats. Has BMS (undated); Miyairi<br />
fruiting bodies of range of hosts and been recorded attacking et al. (1994)<br />
several edible<br />
habitats. Probably mushrooms in the UK.<br />
mushroom species. It occurs wherever<br />
attacking stalks and mushrooms are<br />
eventually turns the grown and where<br />
fruiting body into a slimy hygiene measures<br />
mass.<br />
are insufficient.<br />
Cephalosporium<br />
White mycelium on Cephalosporium Rare in mushrooms in the UK. Fletcher et al. (1994)<br />
spp.<br />
fruiting body gills species can be found<br />
27
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pathogen Synonyms Symptom Notes on worldwide<br />
distribution<br />
all over the world.<br />
Likely to occur<br />
wherever<br />
mushrooms are<br />
grown.<br />
Notes on UK distribution Reference<br />
Fusarium<br />
Damping off Cosmopolitan, Reported causing damping off in Moore (1959)<br />
oxysporum<br />
recorded on a wide the UK. Also present on other<br />
range of hosts and<br />
habitats. Likely to<br />
occur wherever<br />
mushrooms are<br />
grown.<br />
hosts.<br />
Fusarium solani Damping off Cosmopolitan, Reported causing damping off in Moore (1959)<br />
recorded on a wide the UK. Also present on other<br />
range of hosts and<br />
habitats. Likely to<br />
occur wherever<br />
mushrooms are<br />
grown.<br />
hosts.<br />
Hormiactis alba Irregular brown spots Occurs wherever Present in UK mushrooms but Fletcher et al. (1994);<br />
mushrooms are uncommon, not a serious BMS (undated)<br />
grown.<br />
disease<br />
Hypomyces Sepedonium This species can cause Cosmopolitan, Relatively common in Britain on Flegg et al. (1985);<br />
chrysospermus chrysospermum, necrosis on mushroom recorded on a wide a wide range of hosts. Common Fletcher et al. (1994);<br />
Sepedonium tissue but it is more range of hosts and weed mould in UK mushroom Farr et al. (undated);<br />
mycophilum, common as a weed habitats. Reports of it composts.<br />
BMS (undated)<br />
Sporotrichum mould competitor (See infecting mushrooms<br />
mycophilum,<br />
Trichoderma<br />
mycophilum,<br />
Uredo mycophila<br />
Annex Table 2). are rare.<br />
Hypomyces Mycogone<br />
Massively distorted Occurs wherever Present and common on Fletcher et al. (1994);<br />
perniciosus (Wet perniciosa<br />
caps (cauliflower-like) mushrooms are mushroom and also present on BMS (undated)<br />
28
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pathogen Synonyms Symptom Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
bubble)<br />
with drops of amber<br />
liquid, also small<br />
‘bubbles’.<br />
grown. other hosts.<br />
Hypomyces Cladobotryum Rapid mycelial growth Occurs wherever Present and common on Fletcher et al. (1994);<br />
rosellues<br />
dendroides,<br />
over casing and mushrooms are mushroom and also present on BMS (undated)<br />
(Cobweb)<br />
Cladobotryum mushrooms; cap grown.<br />
other hosts.<br />
mycophilum,<br />
Dactylium<br />
dendroides<br />
spotting.<br />
Lecanicillium Cephalosporium Lesions on mushroom Cosmopolitan, Present but only observed Moore (1959); Zare &<br />
psalliotae<br />
curtipes var.<br />
cap.<br />
recorded on a wide occasionally in mushrooms. Gams (2003)<br />
uredinicola,<br />
range of hosts.<br />
Verticillium psalliotae<br />
Possibly occurs<br />
wherever<br />
mushrooms are<br />
grown.<br />
Melanospora Gonatobotrys Only detail is that it was Cosmopolitan, on a Recorded in mushrooms in the BMS (undated); Farr et<br />
damnosa<br />
simplex<br />
found infecting<br />
wide range of hosts. UK, also present on other hosts. al. (undated); Vakili<br />
mushroom in the UK. No reports infecting<br />
mushroom found <strong>for</strong><br />
outside the UK.<br />
(1989)<br />
Mortierella bainieri<br />
Peeling stipe, dark Occurs wherever Present in the UK on a range of Fletcher et al. (1994);<br />
(Shaggy stipe)<br />
brown discolouration, mushrooms are hosts but rare in mushrooms. BMS (undated)<br />
coarse grey-white<br />
mycelium over casing.<br />
grown.<br />
Mycogone rosea White mould of<br />
Reported in Britain, Present in the UK. Has been Moore (1959); BMS<br />
mushroom.<br />
Germany, Uganda, recorded on mushrooms and (undated); Brady &<br />
Hungary and plant hosts. Rare because of Gibson (1976)<br />
Australasia, but current hygiene measures in<br />
probably more widely<br />
distributed in regions<br />
where edible fungi<br />
are cultivated<br />
mushroom growing.<br />
29
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pathogen Synonyms Symptom Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Paecilomyces Spicaria penicillata Isolated from a<br />
Isolated from a No record <strong>for</strong> this species found CABI (undated);<br />
penicillatus<br />
decaying mushroom. decaying mushroom in the UK but it is likely to have a Luangsa-ard et al.<br />
in Belgium. Has been wider presence than that already (2004)<br />
found on decaying<br />
plants and wood. No<br />
other records <strong>for</strong><br />
decaying<br />
mushrooms.<br />
reported.<br />
Penicillium<br />
Penicillium<br />
Isolated from decaying Has been isolated Present, has been observed CABI (undated); BMS<br />
brevicompactum brunneostoloniferum, mushrooms, probably from decaying on/with mushrooms in UK (undated)<br />
Penicillium<br />
also a cause of weed mushrooms in the amongst other hosts/habitats.<br />
brunneostoloniferum, mould (see Annex USA, likely to also<br />
Penicillium<br />
Table 2).<br />
occur with<br />
stoloniferum,<br />
mushrooms<br />
Penicillium<br />
wherever they are<br />
volgaense<br />
grown as the fungus<br />
is cosmopolitan and<br />
occurs on a wide<br />
range of<br />
hosts/habitats.<br />
Simplicillium Cephalosporium The mildew apparently Appears to have a Present in the UK but only Moore (1959); BMS<br />
lamellicola (Gill lamellicola,<br />
does little harm. wide distribution on a observed occasionally on (undated); Pantou et al.<br />
Mildew)<br />
Verticillium<br />
range of hosts and mushrooms.<br />
(2005)<br />
lamellicola<br />
habitats but few<br />
records <strong>for</strong> it on<br />
mushrooms.<br />
Verticillium<br />
Variety of symptoms on Predominant cause Recorded present in the UK but BMS (undated); Collopy<br />
fungicola var.<br />
the cap including of dry bubble in no record <strong>for</strong> mushrooms. et al. (2001); Largeteau<br />
aleophilum<br />
lesions, distortion and North America. Likely<br />
et al. (2004)<br />
discolouration.<br />
to have a wider<br />
distribution on other<br />
hosts.<br />
30
Pathogen Synonyms Symptom Notes on worldwide<br />
distribution<br />
Verticillium<br />
Verticillium<br />
Variety of symptoms Predominant cause<br />
fungicola var. malthousei<br />
including lesions from of dry bubble in<br />
fungicola<br />
the cap, cap distortion Europe. Likely to<br />
and discolouration. have a wider<br />
distribution on other<br />
hosts. Thought to<br />
have recently spread<br />
to North America<br />
from Europe through<br />
the import of material<br />
or machines used <strong>for</strong><br />
mushroom<br />
cultivation.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Recorded on mushrooms in the<br />
UK and common.<br />
Fletcher et al. (1994);<br />
BMS (undated);<br />
Collopy et al. (2001);<br />
Largeteau et al. (2004)<br />
31
Table 2. Weed moulds (fungi) associated with <strong>Agaricus</strong> <strong>bisporus</strong><br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Ascobolus leveillei Ascobolus boudieri,<br />
Likely to be cosmopolitan, in Present in a range of habitats,<br />
Ascozonus leveillei, Boudiera a wide range of countries recorded on mushroom compost<br />
boudieri, Comesia leveillei hosts and habitats. Possibly in the UK in 1935. Rarely occurs<br />
occurs wherever mushrooms now in mushroom composts,<br />
are grown should hygiene probably due to better hygiene.<br />
measures be insufficient. .<br />
Aspergillus spp. Aspergillus species are Aspergillus is a common weed<br />
cosmopolitan, and occur in a mould in the UK mushroom<br />
wide range of countries hosts composts, occurs if hygiene<br />
and habitats. Possibly occurs<br />
wherever mushrooms are<br />
grown should hygiene<br />
measures be insufficient.<br />
measures are insufficient.<br />
Botryotinia fuckeliana Botrytis cinerea, Botrytis Cosmopolitan, on a wide Has been reported on<br />
gemella, Sclerotinia<br />
range of hosts. Possibly mushroom beds in the UK,<br />
fuckeliana<br />
occurs wherever mushrooms probably due to insufficient<br />
are grown should hygiene<br />
measures be insufficient.<br />
hygiene.<br />
Botryotrichum piluliferum Sepedonium albogriseum, Cosmopolitan, on a wide Present in the UK in soil but no<br />
Chaetomium piluliferum range of hosts. Possibly records <strong>for</strong> UK mushroom<br />
occurs wherever mushrooms<br />
are grown should hygiene<br />
measures be insufficient.<br />
Reported to be a cause of<br />
plaster mould in the USA.<br />
composts.<br />
Notes on UK distribution Reference<br />
Moore (1959); BMS<br />
(undated)<br />
Fletcher et al. (1994);<br />
Beyer (2002)<br />
Moore (1959)<br />
Beyer (2002); BMS<br />
(undated)<br />
32
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Cephalotrichum microsporum Stysanus microsporus, Cosmopolitan, on a wide<br />
(Whisker mould)<br />
Doratomyces microsporus range of hosts and habitats.<br />
Whisker mould occurs<br />
wherever mushrooms are<br />
grown should hygiene<br />
measures be insufficient.<br />
Cephalotrichum<br />
purpureofuscum<br />
(Whisker mould)<br />
Cephalotrichum stemonitis<br />
(Whisker mould)<br />
Chaetomium globosum<br />
(Olive green mould)<br />
Chromelosporium fulvum<br />
(Cinnamon brown mould)<br />
Doratomyces<br />
purpureofuscus,<br />
Stysanus purpureofuscus<br />
Doratomyces stemonitis,<br />
Stysanus stemonitis<br />
Chaetomium olivaceum,<br />
Chaetomium subglobosum<br />
Alytosporium fulvum,<br />
Chromelosporium ollare,<br />
Ostracoderma dichotomum,<br />
Trichosporum fulvum, Peziza<br />
ostracoderma<br />
Whisker mould occurs<br />
wherever mushrooms are<br />
grown. This fungus appears<br />
to be cosmopolitan having a<br />
wide host/habitat range.<br />
Whisker mould occurs<br />
wherever mushrooms are<br />
grown. This fungus appears<br />
to be cosmopolitan having a<br />
wide host/habitat range.<br />
Occurs wherever mushrooms<br />
are grown. This fungus<br />
appears to be cosmopolitan<br />
having a wide host/habitat<br />
range.<br />
Occurs wherever mushrooms<br />
are grown. This fungus<br />
appears to be cosmopolitan<br />
having a wide host/habitat<br />
range.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Present in the UK on a wide<br />
range of hosts/habitats although<br />
no records <strong>for</strong> mushrooms.<br />
Likely to occur as part of the<br />
species in the whisker mould<br />
complex which has been<br />
reported in UK mushroom<br />
composts.<br />
Present in the UK on a wide<br />
range of hosts/habitats although<br />
no records <strong>for</strong> mushrooms.<br />
Likely to occur as part of the<br />
species in the whisker mould<br />
complex which has been<br />
reported in UK mushroom<br />
composts.<br />
Present in the UK on a wide<br />
range of hosts/habitats although<br />
no records <strong>for</strong> mushrooms.<br />
Likely to occur as part of the<br />
species in the whisker mould<br />
complex which has been<br />
reported in UK mushrooms.<br />
Present in the UK on a wide<br />
range of hosts/habitats.<br />
Reported to occur in UK<br />
mushroom composts.<br />
Present on a wide range of<br />
hosts, reported in mushroom<br />
beds in the UK.<br />
Beyer (2002); BMS<br />
(undated)<br />
Beyer (2002); BMS<br />
(undated)<br />
Beyer (2002); BMS<br />
(undated)<br />
Farr et al. (undated);<br />
Beyer (2002); BMS<br />
(undated); Moore,<br />
(1959)<br />
Beyer (2002); BMS<br />
(undated)<br />
33
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Chrysosporium merdarium Chrysosporium verruculatum, Reported to be present in<br />
(Yellow mould)<br />
Sporotrichum corii,<br />
mushroom beds wherever<br />
Sporotrichum merdarium, mushrooms are grown. This<br />
Sporotrichum scotophilum fungus appears to be<br />
cosmopolitan having a wide<br />
host/habitat range.<br />
Chrysosporium sulfureum Isaria sulfurea Reported to be present in<br />
(Yellow mould)<br />
mushroom beds wherever<br />
mushrooms are grown.<br />
Clitocybe dealbata<br />
<strong>Agaricus</strong> dealbatus The fungus appears to have<br />
a north temperate distribution<br />
and has a wide host/habitat<br />
range. Possibly occurs<br />
wherever mushrooms are<br />
grown should hygiene<br />
measures be insufficient.<br />
Clitopilus cretatus<br />
<strong>Agaricus</strong> cretatus, Clitopilus Likely to be cosmopolitan,<br />
scyphoides<br />
reported in soils in Europe,<br />
Asia and North America.<br />
Coprinopsis atramentaria<br />
Coprinopsis cinerea<br />
Coprinus atramentarius Coprinopsis or ink cap fungi<br />
are found all over the world.<br />
They have been observed as<br />
a weed mould wherever<br />
mushrooms are grown.<br />
Coprinus fimetarius Coprinopsis or ink cap fungi<br />
are found all over the world.<br />
They have been observed as<br />
a weed mould wherever<br />
mushrooms are grown.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
No records <strong>for</strong> this fungus in the<br />
UK specifically, but it is reported<br />
in several European countries<br />
indicating that it is likely be<br />
present.<br />
Reported as a weed mould in<br />
mushrooms in the UK,<br />
infrequent occurrence.<br />
Present in the UK on a wide<br />
range of hosts/habitats.<br />
Occasionally invades mushroom<br />
beds.<br />
Present in the UK on a wide<br />
range of hosts/habitats and has<br />
also been reported infesting UK<br />
mushroom beds.<br />
Present in the UK on a wide<br />
range of hosts/habitats and has<br />
also been reported infesting UK<br />
mushroom beds.<br />
Present in the UK on a wide<br />
range of hosts/habitats and has<br />
also been reported infesting UK<br />
mushroom beds.<br />
Geels et al. (1988)<br />
Fletcher et al. (1994);<br />
CSL records<br />
Moore (1959); Phillips<br />
(2006)<br />
Moore (1959); BMS<br />
(undated)<br />
CSL Records<br />
Beyer (2002); CSL<br />
Records<br />
34
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Coprinopsis radiata<br />
Coprinus radiatus Coprinopsis or ink cap fungi Present on a wide range of Beyer (2002); CSL<br />
are found all over the world. habitats in the UK, but no record Records<br />
They have been observed as<br />
a weed mould wherever<br />
mushrooms are grown.<br />
of it in UK mushrooms beds.<br />
Coprinus comatus<br />
<strong>Agaricus</strong> comatus, <strong>Agaricus</strong> Coprinopsis or ink cap fungi Present in the UK on a wide CSL Records<br />
cylindricus, <strong>Agaricus</strong><br />
are found all over the world. range of hosts/habitats and has<br />
fimetarius, <strong>Agaricus</strong> ovatus They have been observed as also been reported infesting UK<br />
Coprinus comatus var. a weed mould wherever mushroom beds.<br />
caprimammillatus, Coprinus<br />
comatus var. ovatus,<br />
Coprinus ovatus<br />
mushrooms are grown.<br />
Corticium sp. (identity not<br />
Corticium species are Corticium species are present in Beyer (2002)<br />
known)<br />
present all over the world the UK but no published records<br />
and are common decay <strong>for</strong> its occurrence in UK<br />
agents. Likely to have been<br />
an opportunistic coloniser of<br />
mushroom compost.<br />
mushroom beds.<br />
Corynascus thermophilus Chaetomidium thermophilum, This has been reported on Present in the UK on straw and Beyer (2002); BMS<br />
(Flour mould)<br />
Thielavia thermophila mushroom compost in North straw compost but not reported (undated)<br />
America.<br />
in mushroom compost<br />
specifically.<br />
Diehliomyces microsporus Pseudobalsamia microspora Occurs wherever mushrooms Present, but outbreaks rare due Fletcher et al. (1994);<br />
(False truffle)<br />
are grown.<br />
to improved growing methods. Moore (1959)<br />
35
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Geosmithia emersonii<br />
Penicillium emersonii Isolated from mushroom Present in the UK, but no<br />
compost in the Netherlands, records <strong>for</strong> this species on<br />
likely to be one of many<br />
species classed as smokey<br />
mould. Species appears to<br />
be cosmopolitan, occurring<br />
on a wide range of habitats.<br />
mushroom compost in the UK.<br />
Heleococcum aurantiacum No records found elsewhere. Present in the UK. Has been<br />
recorded in mushroom compost<br />
but this appears to be a rare<br />
occurrence.<br />
Notes on UK distribution Reference<br />
CABI (undated)<br />
Moore (1959); Wood<br />
(1957)<br />
36
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Humicola insolens<br />
This fungus appears to be<br />
cosmopolitan having a wide<br />
host/habitat range.<br />
Hypomyces chrysospermus Sepedonium<br />
Cosmopolitan, on a range of<br />
(yellow mould)<br />
chrysospermum,<br />
hosts and habitats. Appears<br />
Sepedonium mycophilum, to cause yellow mould<br />
Sporotrichum mycophilum, wherever mushrooms are<br />
Trichoderma mycophilum, grown. Also known to be able<br />
Uredo mycophila<br />
to infect mushrooms (Annex<br />
Table 1) but reports of this<br />
are rare.<br />
Mortierella reticulata Reported to be present in<br />
mushroom compost in the<br />
USA. Probably occurs<br />
wherever mushrooms are<br />
grown.<br />
Mucor mucedo<br />
Appears to be cosmopolitan,<br />
it is present on a range of<br />
hosts and habitats in several<br />
continents but there are few<br />
reports in mushroom<br />
compost. Possibly an<br />
opportunistic coloniser of<br />
composts.<br />
Myceliophthora lutea (mat and Chrysosporium luteum, Occurs wherever mushrooms<br />
confetti)<br />
Scopulariopsis lutea<br />
are grown.<br />
Nectria peziza Dialonectria peziza,<br />
Hydropisphaera peziza,<br />
Nectria aurea, Nectria<br />
epigaea, Sphaeria aurea,<br />
Sphaeria peziza<br />
Cosmopolitan, on a wide<br />
range of hosts. Possibly<br />
occurs wherever mushrooms<br />
are grown should hygiene<br />
measures be insufficient.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Present in the UK in mushroom<br />
compost amongst other habitats.<br />
Relatively common in the UK on<br />
a wide range of hosts. Common<br />
weed mould in UK mushroom<br />
composts.<br />
Recorded in mushroom compost<br />
in UK. Appears to be rare in the<br />
UK.<br />
Recorded in mushroom spawn.<br />
Unknown if it was causing a<br />
problem.<br />
Present in the UK, occurs<br />
infrequently in mushroom<br />
composts.<br />
Common in UK on a range of<br />
hosts. Has been reported in<br />
mushroom beds.<br />
CABI (undated); BMS<br />
(undated)<br />
Flegg et al. (1985);<br />
Fletcher et al. (1994);<br />
Farr et al. (undated);<br />
BMS (undated)<br />
CABI (undated); BMS<br />
(undated); Betterley &<br />
Brown (1989)<br />
CABI (undated); Farr et<br />
al. (undated)<br />
Fletcher et al. (1994)<br />
Moore (1959); BMS<br />
(undated)<br />
37
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Neurospora sitophila Cosmopolitan, on a wide Present in the UK and likely to Perkins & Davis (2000);<br />
range of hosts. Possibly occur in mushroom compost – Farr et al. (undated);<br />
occurs wherever mushrooms<br />
are grown.<br />
one unconfirmed CSL record. CSL Records<br />
Oedocephalum fimetarium Haplotrichum fimetarium Reported in North America Rare in the UK. Beyer (2002); HRI<br />
(Brown mould)<br />
and New Zealand but not<br />
common, likely to occur<br />
wherever mushrooms are<br />
grown but major injury to<br />
mushrooms crops is<br />
improbable.<br />
records<br />
Oedocephalum glomerulosum Haplotrichum glomerulosum, Cosmopolitan, on a wide Present in the UK, recorded on BMS (undated); Farr et<br />
(Brown mould)<br />
Mucor glomerulosus, range of hosts. Possibly numerous hosts and habitats al. (undated)<br />
Pyronema omphalodes occurs wherever mushrooms<br />
are grown should hygiene<br />
measures be insufficient.<br />
including mushroom compost.<br />
Panaeolus subbalteatus <strong>Agaricus</strong> subbalteatus, Present in North America, Present and has been recorded Moore (1959); Phillips<br />
(weed panaeolus)<br />
Panaeolus cinctulus<br />
Europe in a wide range of<br />
habitats. Likely to occur<br />
wherever mushrooms are<br />
grown if hygiene measures<br />
are insufficient.<br />
in mushroom compost.<br />
(2006)<br />
Papulaspora byssina<br />
Anamorphic Chaetomium Occurs wherever mushrooms Present and reported to be CABI (undated); Moore<br />
(Brown plaster mould) species<br />
are grown.<br />
common, but comparatively<br />
harmless unless compost is wet<br />
and tight.<br />
(1959); Anon. (2000)<br />
38
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Penicillium brevicompactum Penicillium<br />
Cosmopolitan, on a wide<br />
brunneostoloniferum, range of hosts. Possibly<br />
Penicillium<br />
occurs wherever mushrooms<br />
brunneostoloniferum, are grown if hygiene<br />
Penicillium stoloniferum,<br />
Penicillium volgaense<br />
measures are insufficient.<br />
Penicillium chermesinium<br />
Occurs wherever mushrooms<br />
are grown.<br />
Penicillium spp.<br />
(Smoky mould)<br />
Penicillium species are<br />
ubiquitous and smoky mould<br />
occurs wherever mushrooms<br />
are grown.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Present on many hosts and<br />
habitats in the UK. Observed in<br />
mushroom beds in the UK.<br />
Present in the UK but rare in<br />
mushroom composts.<br />
Smoky mould has been reported<br />
in the UK and is common.<br />
BMS (undated)<br />
Fletcher et al. (1994);<br />
Beyer (2002); BMS<br />
(undated)<br />
Fletcher et al. (1994);<br />
Beyer (2002)<br />
39
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Peziza vesiculosa Helvella vesiculosa, Peziza Present in a range of habitats<br />
lycoperdioides, Scodellina in North America and<br />
vesiculosa, Rhopalomyces<br />
pallidus, Pustularia<br />
vesiculosa, Aleuria<br />
vesiculosa, Oedocephalum<br />
pallidum<br />
Europe.<br />
Podosordaria pedunculata Xylaria vaporaria<br />
There are few records <strong>for</strong> this<br />
species <strong>for</strong> outside the UK<br />
but it is likely to be present<br />
elsewhere.<br />
Pythium hydnosporum<br />
Artotrogus hydnosporus<br />
Pythium artotrogus<br />
Present in mushroom<br />
composts in North America<br />
and Europe.<br />
Pythium oligandrum Cosmopolitan, on a wide<br />
range of hosts. Possibly<br />
occurs wherever mushrooms<br />
are grown should hygiene<br />
Roumegueriella rufula Chaetomium rufulum,<br />
Eurotium insigne, Lilliputia<br />
insignis, Lilliputia rufula,<br />
Mycogala macrospora<br />
Scopulariopsis coprophila<br />
(White plaster mould)<br />
Monilia fimicola,<br />
Monosporium coprophilum,<br />
Scopulariopsis fimicola<br />
measures be insufficient.<br />
Cosmopolitan, on a wide<br />
range of hosts. Possibly<br />
occurs wherever mushrooms<br />
are grown should hygiene<br />
measures be insufficient.<br />
Occurs wherever mushrooms<br />
are grown.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Present in a range of habitats<br />
and has been recorded in<br />
mushroom beds in the UK.<br />
Present on a wide range of<br />
hosts and habitats in the UK.<br />
Due to improved hygiene<br />
measures now less likely to<br />
occur.<br />
Reported as present in the UK<br />
on other hosts. Likely to be a<br />
common occurrence in<br />
mushroom compost.<br />
Reported as present in the UK<br />
on other hosts. Likely to be a<br />
common occurrence in<br />
mushroom compost.<br />
Present in a wide variety of<br />
habitats. Has been reported on<br />
mushroom compost in past.<br />
Probably uncommon now due to<br />
better hygiene.<br />
Recorded on mushroom<br />
compost in the UK. Relatively<br />
common.<br />
Moore (1959); Phillips<br />
(2006)<br />
Moore (1959); BMS<br />
(undated)<br />
Fletcher et al. (1994);<br />
Beyer (2002); Farr et al.<br />
(undated)<br />
Fletcher et al. (1994);<br />
Beyer (2002); Farr et al.<br />
(undated)<br />
Moore (1959); BMS<br />
(undated); Schroers et<br />
al. (1999); CABI<br />
(undated)<br />
Anon (2000); BMS<br />
(undated)<br />
40
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Sporendonema purpurascens Coprotrichum purpurascens, Appears to be present<br />
(Lipstick mould)<br />
Geotrichum purpurascens, wherever mushrooms are<br />
Sporendonema<br />
purpurascens<br />
grown.<br />
Sporotrichum spp. (Plaster or Possibly the perfect stage of Species of Sporotrichum are<br />
Flour mould)<br />
Corticium sp.<br />
found in a variety of habitats<br />
throughout the world.<br />
Trichocladium pyri<strong>for</strong>me Recorded in mushroom<br />
compost in Ireland. Few<br />
records <strong>for</strong> elsewhere. Likely<br />
to be an opportunistic<br />
coloniser of mushroom<br />
Trichoderma aggressivum f.<br />
europaeum<br />
Trichoderma aggressivum f.<br />
aggressivum<br />
compost.<br />
Trichoderma harzinum (Th2) Present in Europe and<br />
relatively common as a<br />
cause of green mould in<br />
mushroom compost.<br />
Trichoderma harzinum (Th4) Present in North America<br />
and relatively common as a<br />
cause of green mould in<br />
mushroom compost.<br />
Trichoderma asperellum Recorded in mushroom<br />
compost in Hungary.<br />
Appears to have a wide<br />
global distribution. Used as a<br />
biocontrol agent.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Present and an occasional<br />
contaminant but not usually<br />
damaging.<br />
Many species of Sporotrichum<br />
are present in the UK in a wide<br />
variety of habitats but no specific<br />
records found <strong>for</strong> mushrooms.<br />
No records <strong>for</strong> this fungus as<br />
present in the UK but present in<br />
soil in Ireland and there<strong>for</strong>e<br />
likely to be present in the UK.<br />
Present and common as a<br />
cause of green mould in<br />
mushroom compost.<br />
There are no records of this<br />
species in the UK. A 2008<br />
HDC-funded limited survey did<br />
not detect it.<br />
No record of this fungus in the<br />
UK.<br />
Moore (1959); van<br />
Greuning & Eicker<br />
(1991)<br />
BMS (undated); Beyer<br />
(2002)<br />
BMS (undated)<br />
Samuels et al. (2002)<br />
Samuels et al. (2002);<br />
Farr et al. (undated);<br />
Lane (2008).<br />
Hatvani et al. (2007)<br />
41
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Trichoderma atroviride Hypocrea atroviridis Occurs wherever mushrooms<br />
are grown. Also present on<br />
other hosts.<br />
Trichoderma harzianum Trichoderma lignorum var. Cosmopolitan on a range of<br />
narcissi,<br />
hosts and habitats Recorded<br />
Trichoderma narcissi in mushroom compost in<br />
Hungary. Probably occurs<br />
wherever mushrooms are<br />
grown. Some strains of T.<br />
harzinum are known to not<br />
cause problems in<br />
mushroom production.<br />
Trichoderma koningii Acrostalagmus koningii North temperate on a range<br />
of hosts and habitats. Likely<br />
to occur in mushroom<br />
compost wherever<br />
mushrooms are produced.<br />
Green mould outbreaks<br />
originally attributed to be this<br />
species might have actually<br />
been caused by a species in<br />
the T. aggressivum complex.<br />
Trichoderma longibrachiatum Cosmopolitan on a range of<br />
hosts and habitats Recorded<br />
in mushroom compost in<br />
Hungary. Probably occurs<br />
wherever mushrooms are<br />
grown.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Present and relatively common<br />
in mushroom compost in the UK.<br />
Present, not known if the strains<br />
recorded on UK mushroom<br />
composts are strains of T.<br />
harzinum or isolates of<br />
Trichoderma aggressivum f.<br />
europaeum.<br />
Present on numerous<br />
hosts/habitats in the UK. One<br />
record in BMS <strong>for</strong> its occurrence<br />
in mushroom compost.<br />
However, in the last decade this<br />
species is only considered to<br />
have caused very minor<br />
problems.<br />
Present in the UK in a wide<br />
variety of habitats. Possibly may<br />
occur in mushroom compost.<br />
Dodd et al. (2003); BMS<br />
(undated)<br />
Hatvani et al. (2007);<br />
BMS (undated)<br />
BMS (undated); Farr et<br />
al. (undated); CABI<br />
(undated)<br />
Seaby (1996); Samuels<br />
(2006).<br />
Hatvani et al. (2007)<br />
42
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Weed mould Synonym Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Trichoderma pseudokoningii Appears to have a<br />
Present, several occurrences in BMS (undated); Farr et<br />
cosmopolitan distribution on mushroom compost. Present on al. (undated); Samuels<br />
a range of hosts and<br />
habitats. Likely to occur<br />
wherever mushrooms are<br />
grown.<br />
other hosts.<br />
(2006);<br />
Trichoderma virens Gliocladium virens,<br />
Cosmopolitan on a range of Present in the UK on a range of CABI (undated); BMS<br />
Hypocrea virens<br />
hosts and habitats, few hosts/habitats. Recently (undated); C. Lane<br />
reports of it causing<br />
recorded as a weed mould in UK (CSL, 2007, Personal<br />
economic loss as a weed causing economic loss.<br />
Communication); Singh<br />
mould in mushroom<br />
production. Reported to be a<br />
weed mould in edible<br />
mushroom production in<br />
India.<br />
et al. (2006)<br />
Trichoderma viride<br />
Hypocrea rufa<br />
Cosmopolitan, on a wide Present on a wide range of Fletcher et al. (1994);<br />
(green mould)<br />
Hypocrea rufa f. sterilis range of hosts. Possibly hosts in the UK. Also relatively BMS (undated); Farr et<br />
Hypocrea rufa var. rufa occurs wherever mushrooms common in mushroom compost. al. (undated); Seaby<br />
Pyrenium lignorum<br />
are grown. Presence However, in the last decade this (1996)<br />
Sphaeria rufa<br />
indicates poor composting. species is considered to only<br />
Trichoderma lignorum Green mould outbreaks have caused very minor<br />
originally attributed to be this<br />
species might have actually<br />
been T. aggressivum.<br />
problems.<br />
Trichophaea abundans Anthracobia humillima, Appears to be cosmopolitan, Present in a range of hosts and Coetzee & Eicker<br />
Dichobotrys abundans, probably occurs on a wide habitats in the UK but no (1994); BMS (undated)<br />
Lachnea abundans,<br />
range of habitats and present records <strong>for</strong> mushroom compost.<br />
Patella abundans<br />
in mushroom compost<br />
wherever mushrooms are<br />
grown. Reported to occur in<br />
mushrooms in South Africa.<br />
Trichothecium roseum Cephalothecium roseum, Appears to be cosmopolitan, Present in a range of hosts and Beyer (2002); Farr et al.<br />
(Plaster or Flour moulds) Hyphelia rosea, Hyphoderma probably occurs on a wide habitats in the UK but no (undated); BMS<br />
43
Weed mould Synonym Notes on worldwide<br />
distribution<br />
roseum, Hypomyces roseus, range of habitats and<br />
Puccinia rosea, Sphaeria probably present in<br />
rosea, Trichoderma roseum mushroom compost<br />
wherever mushrooms are<br />
grown.<br />
Trichurus spiralis<br />
Appears to be cosmopolitan,<br />
(Whisker mould)<br />
probably occurs on a wide<br />
range of habitats and<br />
probably present in<br />
mushroom compost<br />
wherever mushrooms are<br />
grown.<br />
Volvaria sp.<br />
Numerous species of this<br />
genus distributed worldwide.<br />
Some are even cultivated <strong>for</strong><br />
edible mushrooms. It is likely<br />
that this could be a weed<br />
mould should there be the<br />
opportunity.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
records <strong>for</strong> mushroom compost. (undated)<br />
Present in a wide variety of<br />
habitats but not recorded in UK<br />
mushrooms composts.<br />
Several Volvaria species are<br />
present in the UK. Moore (1959)<br />
reported one unidentified<br />
species invading mushroom<br />
beds in Norfolk in 1945. Likely to<br />
be rare with modern hygiene<br />
measures.<br />
Beyer (2002); Farr et al.<br />
(undated); BMS<br />
(undated)<br />
Moore (1959)<br />
44
Table 3. Bacterial pathogens associated with <strong>Agaricus</strong> <strong>bisporus</strong><br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pathogen Symptom Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Bacterial pit, agent not known Small dark slimy pits on Wherever mushrooms are Common in mushrooms. Fletcher et al. (1994)<br />
caps.<br />
grown.<br />
Burkholderia gladioli pv.<br />
Soft rot, mild lesions to Present in mushrooms in Common, with sporadic<br />
Gill & Tsuneda (1997);<br />
agaricicola<br />
deep pitting on caps. New Zealand, Europe. outbreaks occurring in<br />
Chowdhury &<br />
[syn. Pseudomonas cepacia]<br />
(Cavity disease)<br />
mushrooms crops.<br />
Heinemann (2006)<br />
Ewingella americana Browning in the centre of Reported to be associated First discovered on mushrooms Inglis & Peberdy (1996);<br />
the stipes and may be with mushrooms in Spain. in the UK but now considered Reyes et al. (2004)<br />
accompanied by the<br />
collapse of internal<br />
tissues.<br />
uncommon.<br />
Janthinobacterium<br />
Soft rot of cap. Reported originally in the UK Outbreaks in mushroom crops Lincoln et al. (1999)<br />
agaricidamnosum<br />
and France, now considered are rare.<br />
(Soft rot)<br />
present wherever<br />
mushrooms are grown.<br />
Pseudomonas agarici<br />
Gills underdeveloped with Reported in the UK and New Rare, but when found in Fletcher et al. (1994),<br />
(Drippy gill)<br />
creamy-white ooze on Zealand, now considered mushrooms most severe in<br />
decayed areas.<br />
present wherever<br />
mushrooms are grown.<br />
autumn and winter.<br />
Pseudomonas costantinii Brown blotches on cap. Originally found in Finland No record in UK mushroom Munsch et al. (2002)<br />
but the present distribution is<br />
unknown. Originally<br />
considered a strain of<br />
Pseudomonas tolaasii.<br />
crops.<br />
Pseudomonas fluorescens Possibly associated with Not known but reported in a Not known but no record of it in Anon. (2004)<br />
biotype G (Bacterial blotch) mummy disease.<br />
Canadian guidebook. UK mushroom crops.<br />
Pseudomonas fluorescens<br />
strains are present in the UK.<br />
Pseudomonas gingeri<br />
Ginger blotches on cap. Occurs wherever mushrooms Uncommon in mushrooms in the Fletcher et al. (1994)<br />
(Ginger blotch)<br />
are grown.<br />
UK.<br />
45
Pathogen Symptom Notes on worldwide<br />
distribution<br />
Pseudomonas ‘reactans’ Mild infection and P. ‘reactans’ strains<br />
superficial light brown pathogenic to mushroom<br />
discoloration.<br />
were originally reported in<br />
the USA.<br />
Pseudomonas sp./spp.<br />
Mushroom dries out and Mummy disease has been<br />
(Mummy and false mummy discolours; basal swelling observed worldwide but<br />
disease)<br />
of stipes.<br />
outbreaks are rare.<br />
Possibly includes Pseudomonas<br />
aeruginosa<br />
Pseudomonas tolaasii<br />
(Bacterial or Brown blotch)<br />
Brown blotches on cap;<br />
distortion and splitting.<br />
Wherever mushrooms are<br />
grown.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Not known but no record in UK<br />
mushroom crops.<br />
Mummy disease has been<br />
observed in the UK but<br />
outbreaks are rare.<br />
Common on mushrooms in the<br />
UK.<br />
Wells et al. (1996)<br />
Fletcher et al. (1994)<br />
Fletcher et al. (1994)<br />
46
Table 4. Viral pathogens associated with <strong>Agaricus</strong> <strong>bisporus</strong><br />
Pathogen Synonyms Symptoms Notes on worldwide<br />
distribution<br />
<strong>Agaricus</strong> <strong>bisporus</strong><br />
Part of the MVX Part of the MVX<br />
Endornavirus 1<br />
complex.<br />
complex found in<br />
Possibly no<br />
symptoms in<br />
isolation from<br />
other viruses.<br />
Europe.<br />
La France Isometric Virus AbV-4,<br />
Die back, yield Wherever mushrooms<br />
(LIV)<br />
Dieback, La loss, drumstick are grown.<br />
France disease, shaped<br />
MV4, Mushroom mushrooms,<br />
virus 4<br />
discolouration.<br />
Mushroom bacilli<strong>for</strong>m Mushroom virus 3 None Probably wherever<br />
virus (MBV)<br />
mushrooms are grown.<br />
Mushroom virus X<br />
(disease complex of<br />
several viruses)<br />
Bare patches on<br />
beds; brown<br />
caps; crop loss.<br />
Symptoms observed in<br />
Europe.<br />
Vesicle virus None Probably wherever<br />
mushrooms are grown.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Sporadic infections. P.R. Mills (2007,<br />
Warwick HRI, Personal<br />
Communication)<br />
Present but uncommon in the<br />
UK.<br />
Present but uncommon in the<br />
UK. Usually occurs with LIV.<br />
First found in the UK, sporadic<br />
infections occur.<br />
Fletcher et al. (1994)<br />
P.R. Mills (2007,<br />
Warwick HRI, Personal<br />
Communication)<br />
Grogan et al. (2003)<br />
Likely to be present. P.R. Mills (2007,<br />
Warwick HRI, Personal<br />
Communication)<br />
47
Table 5. Insect pests associated with <strong>Agaricus</strong> <strong>bisporus</strong> worldwide<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pest Component attacked Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Lycoriella castanescens<br />
(Sciarid)<br />
Compost, stipe Worldwide Common. Fletcher et al. (1994)<br />
Lycoriella ingenua<br />
(Sciarid)<br />
Compost, stipe Worldwide Common. Fletcher et al. (1994)<br />
Bradysia dif<strong>for</strong>mis Compost, stipe Worldwide Common in the UK but rare in Menzel et al. (2003)<br />
(Sciarid)<br />
mushroom crops.<br />
Bradysia lutaria<br />
(Sciarid)<br />
Compost Worldwide Rare as a pest of mushrooms. White & Smith (2000)<br />
Bradysia matogrossensis<br />
(Sciarid)<br />
Compost Brazil Absent, not known in UK. Fletcher et al. (1994)<br />
Bradysia ocellaris Compost Worldwide Common but rare in mushroom Menzel et al. (2003)<br />
(Sciarid)<br />
crops.<br />
Megaselia bovista<br />
(Phorid)<br />
Mycelium Worldwide Rare in mushroom crops. Anon. (2000)<br />
Megaselia halterata<br />
(Phorid)<br />
Mycelium Worldwide Common. Fletcher et al. (1994)<br />
Megaselia nigra<br />
Mycelium, stipe, cap Worldwide Common in UK but rare in mushroom Fletcher et al. (1994)<br />
(Phorid)<br />
crops.<br />
Megaselia scalaris Mycelium Iran Common in UK but rare in mushroom Zamani et al. (2005)<br />
(Phorid)<br />
crops.<br />
Henria psalliotae<br />
Mycelium, stipe, cap Worldwide<br />
Common but uncommon as a pest in Fletcher et al. (1994)<br />
(Cecid)<br />
Heteropeza pygmaea<br />
(Cecid)<br />
Mycophila speyeri<br />
(Cecid)<br />
Mycophila barnesi<br />
(Cecid)<br />
Lestremia cinerea<br />
(Cecid)<br />
mushroom crops.<br />
48
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pest Component attacked Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Lestremia leucophaea<br />
(Cecid)<br />
Base of stipe Worldwide Now a rare pest in UK. Fletcher et al. (1994)<br />
Achorutes armatus Mycelium, stipe, cap, Worldwide Occasional pest. Fletcher et al. (1994)<br />
(Collembola)<br />
Drosophila funebris<br />
(Fruit fly)<br />
wet compost<br />
Compost, cap Worldwide Occasional pest. Fletcher et al. (1994)<br />
Pullimosina heteroneura<br />
(Sphaerocerid)<br />
Compost Worldwide Occasional pest. Fletcher et al. (1994)<br />
Colboldia fuscipes<br />
(Scatopsid)<br />
Compost Worldwide Occasional pest. Fletcher et al. (1994)<br />
Diplopoda spp.<br />
(Millipede)<br />
Stipe, compost Worldwide Rare. Fletcher et al. (1994)<br />
49
Table 6. Acarina (Mites) associated with <strong>Agaricus</strong> <strong>bisporus</strong><br />
Pest<br />
Order: Prostigmata<br />
Component attacked Notes on worldwide<br />
distribution<br />
Dolichocybe keiferi<br />
Krantz<br />
Brennandania lambi<br />
Krczal<br />
(Australian mushroom<br />
pygmy mite)<br />
Linopodes antennaepes<br />
Banks<br />
Pediculaster<br />
fletchmanni (Wicht)<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Mycophagous. USA Absent Wicht (1970)<br />
Reported to attack mycelia. Australia Absent Gao & Zou (2001)<br />
Mycophagous. Europe Common on mushrooms Anon. (2000)<br />
Feed on weed moulds, and<br />
an indicator of Trichoderma.<br />
Can be a cause <strong>for</strong> crop<br />
rejection due to their bright<br />
colour. Can be a nuisance<br />
to pickers and is known to<br />
cause allergies in humans<br />
but is otherwise harmless to<br />
mushrooms.<br />
Brazil Absent Wicht (1970)<br />
50
Pest Component attacked Notes on worldwide<br />
distribution<br />
Pygmephorus spp. Feed on weed moulds, and Worldwide<br />
(Red Pepper Mites) are indicators of<br />
Trichoderma. Can cause<br />
Specifically:<br />
crop rejection Due to<br />
contamination with their<br />
P. mesembrinae bright red bodies and be Worldwide<br />
Canestrini<br />
can a nuisance to pickers.<br />
Pygmephorus sellnicki is<br />
P. sellnicki Krczal reported to cause allergies<br />
in humans but is otherwise<br />
Worldwide<br />
P. tarsalis Hirst<br />
harmless to mushrooms. Worldwide<br />
P. athiasae Wicht<br />
P. allmanni Krczal<br />
P. kneeboni Wicht<br />
P. quadratus Ewing<br />
P. murphyi Smiley<br />
France<br />
Australia, New<br />
Zealand<br />
USA<br />
USA, Germany<br />
USA<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Widespread on other hosts in<br />
the UK, rare in mushroom<br />
crops but potentially<br />
damaging.<br />
Present<br />
Present<br />
Present<br />
Absent<br />
Absent<br />
Absent<br />
Smiley (1978) reported this as<br />
present in England but the<br />
species is not reported in the<br />
UK checklist or Zoological<br />
Record.<br />
Absent<br />
Gurney & Hussey (1967);Fletcher et al.<br />
(1994); Anon. (2000); Geels et al.<br />
(1988); Flegg et al. (1985)<br />
Wicht (1970)<br />
Gurney & Hussey (1967)<br />
Wicht (1970)<br />
Smiley (1978)<br />
Smiley (1978)<br />
51
Pest Component attacked Notes on worldwide<br />
distribution<br />
Tarsonemus spp. Feed on the mycelial Species of<br />
threads at the base of the Tarsonemus can be<br />
Specifically:<br />
stem causing stems found all over the<br />
damage and discolouration.<br />
Virus vectors.<br />
world.<br />
T. floricolus (Canestrini<br />
& Fanzago)<br />
T. myceliophagus<br />
Hussey<br />
Order: Astigmata<br />
Caloglyphus<br />
mycophagus Megnin<br />
Caloglyphus<br />
mycophagus Megnin<br />
Tyrophagus<br />
putrescentiae<br />
(syn. Tyrophagus<br />
lintneri)<br />
Order: Mesostigmata<br />
Parasitus fimetorum<br />
Berlese<br />
Digamasellus fallax<br />
Leitner<br />
Seven species of<br />
Tarsonemid mite have been<br />
recorded in association with<br />
mushroom crops<br />
Mycophagous Worldwide.<br />
Mycophagous Worldwide.<br />
Mycophagous and feeds on<br />
mushroom mycelium and<br />
tissue as well as moulds<br />
and a variety of organic<br />
material. If present in large<br />
numbers, can results in<br />
both large and small pits on<br />
the mushrooms caps.<br />
Worldwide.<br />
Predatory mite Worldwide.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Both T. floricolus and T.<br />
myceliophagus are present in<br />
the UK.<br />
Geels et al. (1988); Hussey (1963);<br />
Flegg et al. (1985)<br />
Common on mushrooms. Fletcher et al. (1994); Anon. (2000)<br />
Common on mushrooms. Fletcher et al. (1994); Anon. (2000)<br />
Common on mushrooms Fletcher et al. (1994); Anon. (2000)<br />
Common in Mushrooms. Fletcher et al. (1994)<br />
Predatory mite Worldwide. Not known to be present in the<br />
UK.<br />
J. Ostojia-Starzewski, (CSL, Personal<br />
Communication)<br />
52
Pest Component attacked Notes on worldwide<br />
distribution<br />
Arctoseius cetratus<br />
Sellnick<br />
Predatory mite Worldwide.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK distribution Reference<br />
Common in mushrooms where<br />
prey is present. Prey consists<br />
of other invertebrates.<br />
Dendrolaelaps spp. Predatory mite Worldwide. Common in mushrooms where<br />
prey is present. Prey consists<br />
Macrocheles spp. Predatory mite Worldwide.<br />
of other invertebrates.<br />
Common in mushrooms where<br />
prey is present. Prey consists<br />
of other invertebrates.<br />
Fletcher et al. (1994)<br />
Anon. (2000)<br />
Anon. (2000)<br />
53
Table 7. Mycophagous nematode pests associated with <strong>Agaricus</strong> <strong>bisporus</strong><br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pest Component attacked Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Aphelenchoides agarici Mycelium India No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides asterocaudatus Mycelium India No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides bicaudatus Mycelium Australia, Europe No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides coffeae Mycelium Australia No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides composticola Mycelium<br />
Worldwide. Considered with Present but rare in UK mushroom Fletcher et al. (1994)<br />
D. myceliophagus, to be one crops but potentially very<br />
of the two major species of<br />
mycophagous nematodes<br />
affecting mushroom<br />
production worldwide.<br />
damaging.<br />
Aphelenchoides cyrtus Mycelium Germany No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides dactylocercus Mycelium Europe, India Present in the UK on other hosts, Richardson & Grewal<br />
no records found <strong>for</strong> mushrooms (1993); Perper &<br />
Petriello (1977)<br />
Aphelenchoides helophilus Mycelium Europe No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides limberi Mycelium Europe, North America, Asia No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides minor Mycelium India No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides myceliophagus Mycelium India No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides neocomposticola Mycelium India No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides parientinus Mycelium Europe Present but no records associated Richardson & Grewal<br />
with mushrooms <strong>for</strong> UK<br />
(1993); Hodda (2003)<br />
54
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pest Component attacked Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Aphelenchoides richardsoni Mycelium UK Present on mushrooms in UK. Grewal et al. (1992)<br />
Aphelenchoides sacchari Mycelium Europe, India No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993);<br />
Sharma et al. (1981)<br />
Aphelenchoides saprophilus Mycelium Europe, Australia Present but no records associated Richardson & Grewal<br />
with mushrooms <strong>for</strong> UK.<br />
(1993); CSL Nematode<br />
Checklist (undated)<br />
Aphelenchoides spinosus Mycelium Germany, Australia No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Aphelenchoides subtenuis Mycelium Europe, Israel, Australia, Present but no records associated Richardson & Grewal<br />
India<br />
with mushrooms <strong>for</strong> UK.<br />
(1993); Hodda (2003)<br />
Aphelenchoides swarupi Mycelium India, Italy No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993); Hodda (2003)<br />
Aphelenchus avenae Mycelium Europe, Australia Present on mushrooms in the UK. Hooper (1962)<br />
Ditylenchus destructor Mycelium, but considered Worldwide Present but usually associated with Richardson & Grewal<br />
less capable of destroying<br />
other hosts.<br />
(1993); CABI<br />
mushroom mycelium than<br />
D. myceliophagus<br />
Compendium (undated)<br />
Ditylenchus dipsaci Mycelium Worldwide Present but usually associated with Richardson & Grewal<br />
other hosts in the UK.<br />
(1993); CABI<br />
Compendium (undated)<br />
Ditylenchus filimus Mycelium Canada No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Ditylenchus intermedius Mycelium Europe, North America No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Ditylenchus myceliophagus Mycelium<br />
Worldwide. Considered with Rare in UK mushroom crops but Fletcher et al. (1994)<br />
A. composticola, to be one of potentially very damaging – the<br />
the two major species of only Ditylenchus species<br />
mycophagous nematodes considered economically important<br />
affecting mushroom<br />
in commercial mushroom<br />
production worldwide. production according to<br />
Richardson & Grewal (1993).<br />
55
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pest Component attacked Notes on worldwide<br />
distribution<br />
Notes on UK distribution Reference<br />
Ditylenchus valveus Mycelium North America, Asia No UK record <strong>for</strong> this species. Richardson & Grewal<br />
(1993)<br />
Filenchus misellus<br />
Observed experimentally<br />
to eat mushroom mycelia.<br />
No natural records known.<br />
Asia No UK record <strong>for</strong> this species. Okada & Kadota (2002)<br />
Paraphelenchus myceliophthorus Mycelium England, India, Bulgaria Present on mushrooms in UK. Goodey (1958)<br />
Table 8. Saprophytic nematodes associated with <strong>Agaricus</strong> <strong>bisporus</strong> worldwide<br />
Pest Component attacked Notes on worldwide<br />
Notes on UK<br />
distribution<br />
Distribution<br />
Acrobeloides apiculatus Indirect effect on mushroom Worldwide. No UK record <strong>for</strong> this<br />
production – either through the<br />
release of toxins into the compost<br />
or facilitating the rapid and<br />
thorough bacterial colonisation of<br />
the compost.<br />
species.<br />
Acrobeloides buetschlii Indirect effect on mushroom Worldwide. No UK record <strong>for</strong> this<br />
production – either through the<br />
release of toxins into the compost<br />
or facilitating the rapid and<br />
thorough bacterial colonisation of<br />
the compost.<br />
species.<br />
Bursilla spp. Reported as saprophytic in Species of Bursilla can be No UK record known <strong>for</strong><br />
mushrooms compost but affect on found worldwide.<br />
this genus on mushrooms<br />
yield uncertain.<br />
but species of this genus<br />
are likely to be present in<br />
the UK.<br />
Reference<br />
Coles (2002)<br />
Coles (2002)<br />
Richardson & Grewal<br />
(1990)<br />
56
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pest Component attacked Notes on worldwide<br />
Notes on UK<br />
Reference<br />
distribution<br />
Distribution<br />
Caenorhabditis elegans If the nematode establishes it can Worldwide. Most frequently found Richardson & Grewal<br />
rapidly inhibit mycelial growth.<br />
saprobe in the UK (1990)<br />
Complex relationship with<br />
bacterial species, which in some<br />
instances results in abnormal<br />
flushing patterns and mushroom<br />
distortion.<br />
mushroom industry.<br />
Mesorhabditis spp. Reported as saprophytic in Species of Mesorhabditis can No UK record known <strong>for</strong> Jin et al. (2006)<br />
mushrooms compost but affect on be found worldwide, reported this genus on mushrooms<br />
yield uncertain.<br />
with mushrooms in China. but Mesorhabditis are<br />
found in the UK in other<br />
habitats.<br />
Panagrolaimus rigidus Indirect effect on mushroom Worldwide. Unconfirmed record <strong>for</strong> Coles (2002); CABI<br />
production – either through the<br />
release of toxins into the compost<br />
or facilitating the rapid and<br />
thorough bacterial colonisation of<br />
the compost.<br />
UK (no details of host). Compendium (undated)<br />
Pellioditis sp. Reported to have a harmful effect Species of Pellioditis can be No UK record known <strong>for</strong> Jin et al. (2006)<br />
– no further details.<br />
found worldwide; this<br />
this genus on<br />
unidentified species was<br />
reported with mushrooms in<br />
China.<br />
mushrooms.<br />
Pelodera (Cylindridera) icosiensis Reported with mushrooms but Reported with mushrooms in No UK record <strong>for</strong> this Liang et al. (1983)<br />
effects uncertain.<br />
China.<br />
species.<br />
Pelodera strongyloides Indirect effect on mushroom Worldwide distribution. Present but no record Coles (2002); Behnke et<br />
production – either through the<br />
release of toxins into the compost<br />
or facilitating the rapid and<br />
thorough bacterial colonisation of<br />
the compost.<br />
with mushrooms.<br />
al. (1999)<br />
57
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Pest Component attacked Notes on worldwide<br />
Notes on UK<br />
Reference<br />
distribution<br />
Distribution<br />
Pelodera lambdiensis Vector of bacterial diseases of Reported on mushrooms beds No UK record <strong>for</strong> this<br />
mushrooms.<br />
in USA, but reported in other<br />
hosts in Australia, Fiji and<br />
North Africa.<br />
species.<br />
Prodontorhaditis sp. Reported to have a harmful effect Reported with mushrooms in No UK record <strong>for</strong> this Jin et al. (2006)<br />
– no further details.<br />
China.<br />
species.<br />
Rhabditella spp. Reported as saprophytic in Species of Rhabditella can be No UK record known <strong>for</strong><br />
mushrooms compost but affect on found worldwide.<br />
this genus on<br />
yield uncertain.<br />
mushrooms.<br />
Rhabditis (Cephaloboides) Indirect effect on mushroom Not known. No UK record known <strong>for</strong> Coles (2002)<br />
oxycera<br />
production – either through the<br />
release of toxins into the compost<br />
or facilitating the rapid and<br />
thorough bacterial colonisation of<br />
the compost.<br />
this species.<br />
Rhabditis (Choriorhabditis) Indirect effect on mushroom Not known. No UK record known <strong>for</strong> Coles (2002)<br />
longicaudatus<br />
production – either through the<br />
release of toxins into the compost<br />
or facilitating the rapid and<br />
thorough bacterial colonisation of<br />
the compost.<br />
this species.<br />
Rhabditis (Pellioditis) pellio Indirect effect on mushroom Worldwide. No UK record known <strong>for</strong> Coles (2002)<br />
production – either through the<br />
release of toxins into the compost<br />
or facilitating the rapid and<br />
thorough bacterial colonisation of<br />
the compost.<br />
this species.<br />
Rhabditis terricola Indirect effect on mushroom<br />
production – either through the<br />
release of toxins into the compost<br />
or facilitating the rapid and<br />
thorough bacterial colonisation of<br />
the compost.<br />
Not known. Not known. Coles (2002)<br />
Coles (2002); Steiner<br />
(1933)<br />
Richardson & Grewal<br />
(1993)<br />
58
Pest Component attacked Notes on worldwide<br />
distribution<br />
Rhabditis cucumeris Can suppress the development of Worldwide, but reported with<br />
mushroom mycelium,<br />
bacterivorous nematode possibly<br />
an indirect affect.<br />
mushrooms in Poland.<br />
Trilabiatus sp. Reported with mushrooms but Reported with mushrooms in<br />
effects uncertain.<br />
China.<br />
<strong>Commodity</strong> <strong>PRA</strong> <strong>for</strong> Mushrooms<br />
CSL/Warwick HRI, December 18th 2007; revised 24 February 2009<br />
CSL Registered File No. PPP 12011A<br />
Notes on UK<br />
Distribution<br />
No UK record known <strong>for</strong><br />
this species.<br />
No UK record known <strong>for</strong><br />
this genus on<br />
mushrooms.<br />
Reference<br />
Dmowska et al. (1997)<br />
Liang et al. (1983)<br />
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