The use of chemicals, antagonists, repellents and physical barriers for the control of Lycoriella auripila (Diptera: Sciaridae), a pest of the cultivated mushroom Agaricus bisporus

The sciarid, Lycoriella auripila, is a serious pest of commercial mushroom production. A series of trials demonstrated that the use of early, specifically-targeted, treatments of insecticides and/or antagonists and repellents, which distance treatment time from crop harvest, have the potential to play a useful part in the control of initial and subsequent generations of this pest. Of the treatments examined, those involving a drench treatment of the compost at filling (before pasteurisation) proved to be the most effective. Cyromazine and diflubenzuron were the most active insecticides tested, with cyromazine achieving a superior level of control of the initial infestation. Repellents and antifeedants were also effective, with calcium oxalate and sinapic acid both achieving about 50% control when applied at filling. Treatments applied later during the production cycle, unless in combination with a treatment at filling, were progressively less effective at controlling both the initial sciarid infestation and later generations of larvae. Multiple treatments caused greater reductions in fly populations than did the single treatments and continued to do so throughout the cropping cycle, the greatest reduction in the initial generation (79%) occurring with a triple treatment of cyromazine. With the exception of some diflubenzuron treatments, those that were effective resulted in increases in yield. The use of a physical paper barrier caused significant increases in both fly numbers and total yield.     

The effect of sciarid larvae (Lycoriella auripila) on cropping of the cultivated mushroom (Agaricus bisporus)

Significant linear relationships between the mean number of sciarid, Lycoriella auripila, larvae/125 g-sample of casing and yield, numbers of mushrooms and weight/mushroom were demonstrated at all stages of a mushroom crop. Negative relationships were obtained for yield throughout the cropping period. There was no injury threshold for this pest, although an economic threshold of one larva/sample was deduced. Loss in yield was mostly due to the destruction of mushroom primordia and presumed interruption of nutrient supply to the developing sporophores. Numbers of mushrooms were severely reduced in the first, second and third flushes, more so than yield, although a large increase in numbers was demonstrated in the fourth flush. The size of mushroom was inversely related to numbers, although the increases in size in the first three flushes were insufficient to compensate for the reduction in numbers. A reduction in size was evident in the fourth flush.     

Comparative effects of Steinernema feltiae (Nematoda: Steinernematidae) and insecticides on yield and cropping of the mushroom Agaricus bisporus

In a mushroom crop (Agaricus bisporus) affected by a very low level of sciarid fly (Lycoriella auripila) infestation, the effects of an indigenous isolate of insect-parasitic nematode (Steinernema feltiae) and of two commonly used insecticides (diazinon and diflubenzuron) were studied. When compared with untreated plots, nematodes applied to the casing had no adverse effects on mushroom yields whereas insecticides decreased yields. At a rate of 3 × 10⁶ infective juveniles per tray (surface area = 0.56 m²), S. feltiae elicited increases of 28.5% and 19% in the mean total numbers and weights of mushrooms respectively. Treatment only with diflubenzuron resulted in 14.6% and 6% reductions in mean total numbers and weights of mushrooms, respectively; treatment with both diazinon and diflubenzuron caused 18.5% and 9.4% losses. Application of nematodes generally reduced the mean weight per mushroom whereas insecticides increased it; nematodes delayed the onset of mushroom production (first flush) whereas diflubenzuron delayed the third and fourth flushes. Nematode contamination of sporophores was minimal when S. feltiae was applied at casing. Although their numbers declined with time, the nematodes persisted, in the casing layer, throughout the cropping period of seven weeks. It is concluded that yield benefits associated with nematode application can result mainly from nematode effects on A. bisporus and not solely from suppression of a damaging pest population.     

Comparative Assessment of biological (Nematoda: Steinernema feltiae) and chemical methods of control for the mushroom fly Lycoriella auripila (Diptera: Sciaridae)

The sciarid fly Lycoriella auripila is the major pest of mushrooms cultivated in the UK. Its larvae, which are capable of damaging the crop at all stages of production, may cause severe yield losses and can only be controlled with chemical pesticides. An indigenous isolate of the insect‐parasitic nematode Steinemema feltiae was tested as a biological control agent and its effects compared with two commonly used insecticides, diazinon and diflubenzuron. The timing of application of nematodes was found to affect their efficacy. When applied to compost during spawning, nematodes did not significantly reduce fly emergence, but they did if applied at casing when they were almost as effective as diflubenzuron. Diazinon incorporated into compost did not reduce fly emergence and was also the only treatment that did not lower the incidence of mushrooms spoiled by tunnelling of the larvae of L. auripila. When compared with untreated control plots those treated both with diazinon and diflubenzuron showed significant mean losses in yield of 10% in total weight and 17% in total numbers of mushrooms picked. In contrast, when S. feltiae was applied at casing significant mean increases in yield of 7% and 19%, respectively, were attained. Infective nematodes persisted well in casing, very few were found on sporophores.     

Bendiocarb and diflubenzuron as substitute insecticides for endosulfan in commercial mushroom growing

Diflubenzuron and bendiocarb treatments of compost and casing soil at a rate of 1 g a.i./m² each, resulted in comparable or even improved compost and casing soil colonisation over endosulfan treatments (at a rate of 1.5 g a.i./m²). Alternating diflubenzuron/bendiocarb treatments were preferable to the reverse treatments, which tended to diminish total yield of mushrooms significantly by 1.4–3.9 kg/m². This effect was due to the casing soil treatment with diflubenzuron and not due to the compost treatment with bendiocarb after spawning. The effectiveness of these substitutes for endosulfan was tested on five commercial mushroom farms, where a similar or improved control of Megaselia halterata (Diptera: Phoridae) was obtained over control (endosulfan) treatments. If present, Lycoriella auripila (Diptera: Lycoriidae) was very effectively controlled by the substitute insecticides compared with endosulfan. Relatively high numbers of M. halterata were occasionally observed in endosulfan-treated houses, indicating that a certain level of resistance towards this insecticide may already have developed. This assessment of tolerance in M. halterata emphasised the need for substitute insecticides with different modes of action, in addition to environmental reasons. The chemicals should be alternately applied within individual crops to avoid resistance development.     

Control of the mushroom pests Lycoriella auripila (Diptera: Sciaridae) and Megaselia halterata (Diptera: Phoridae) by Steinernema feltiae (Nematoda: Steinernematidae) in field experiments

The nematode Steinernema feltiae (Nematoda: Steinemematidae) was tested for its ability to control two main mushroom pests i.e. the sciarid Lycoriella auripila (Diptera: Sciaridae) and the phorid Megaselia halterata (Diptera: Phoridae) in growing-rooms filled with spawned compost. A clear difference between female and male sciarid control was observed. A nematode application 1 day after casing preceded by an application 1 day before casing on the compost caused an almost complete control (97%) of the F1-generation of female sciarids. The F2-generation of females was similarly controlled (95%) by an application 7 days after casing. A dosage of 1 × 10⁶nematodes m^-2was found to be equally effective as higher dosages. Diflubenzuron remained active throughout entire the cropping period with high sciarid mortality rates varying from 72% to 99%. Phorid control was variable and seemed to depend on the presence of sciarids. In one occasion the control rate of F2-generation phorid larvae was 75% and was possibly caused by the presence of new infective juvenile nematodes recycled in F2-generation sciarid larvae. Diflubenzuron did not significantly reduce phorid numbers.     

Effects of Entomopathogenic Nematodes on Control of a Mushroom-infesting Sciarid Fly and on Mushroom Production

The entomopathogenic nematodes Steinernema feltiae (Biosys strain #27) and Heterorhabditis heliothidis were evaluated for the larval control of a mushroom-infesting sciarid, Lycoriella mali, and for the effects of these nematodes on mushroom (Agaricus bisporus) production. In a series of small-scale mushroom crops, infective-stage H. heliothidis and S. feltiae were applied to the mushroom casing surface in the irrigation water or incorporated into the casing material at densities ranging from 28 to 1120 and 11 to 1120 nematodes cm-2 of casing surface respectively. The mortality of L. mali larvae ranged from 52 to 100% for H. heliothidis and 38 to 100% for S. feltiae. Both nematode species reduced mycelial coverage on the casing surface at primordia initiation. Neither mushroom strain (off-white or white hybrid) or method of application (incorporation into or irrigation onto the casing surface) altered the effect on mycelial coverage. The nematodes's negative effect on mycelial growth confounded the benefit of fly control. At high nematode densities (up to 1120 nematodes cm-2), damage-free mushroom yields for the first week of harvest were less than those from the untreated control. However, at lower nematode densities, at or below 140 cm-2, the nematodes had less effect on mushroom growth, and consequently, damage-free mushroom yields for the first week of harvest were frequently greater than those from the untreated control. In the absence of flies, the first-week mushroom yield generally declined with increasing nematode densities for both white and off-white mushroom hybrids. After 4 weeks of harvest, accumulated mushroom yields had nearly recovered from the earlier decline.     

Susceptibility of mushroom pests to the insect-parasitic nematodes Steinernema feltiae and Heterorhabditis heliothidis

The potential of two species of insect-parasitic rhabditid nematodes (Steinernema feltiae, Heterorhabditis heliothidis) for biological control of mushroom flies was studied in pot trials. Three Diptera that commonly infest mushroom crops were used; the larvae of Megaselia halterata (Phoridae), Heteropeza pygmaea (Cecidomyiidae) and Lycoriella auripila (Sciaridae) were all susceptible to parasitism by both nematode species. Fewer adult phorids and sciarids emerged when compost was nematode-treated and, for L. auripila, the effects of nematode applications at spawning, casing or on both occasions were compared. Casing treatments were more effective than spawning treatments; little extra benefit was gained from applying the nematodes twice. Populations of paedogenetic larvae of H. pygmaea built up rapidly in untreated compost, but were reduced when S. feltiae was applied, and were eradicated by H. heliothidis. Because they can penetrate insect cuticle, as well as natural body openings, Heterorhabditis spp. may be more suitable than Steinernema spp. for the control of mushroom fly larvae.     

Evaluation of a genetically selected strain of Steinernema feltiae against the mushroom sciarid Lycoriella mali

The control potential of a strain (ScP) of Steinernema feltiae genetically selected against the mushroom sciarid Lycoriella solani, was evaluated for the management of L. mali. Trials were conducted at two commercial mushroom farms with high and low levels of fly infestation. The efficacy of the ScP strain was compared with the SN strain of S. feltiae and the chitin synthesis inhibitor, diflubenzuron. At low densities of L. mali, the two strains did not differ in efficacy and caused 85–94% reduction in fly populations. At high fly densities with a mixed infestation of the phorid fly, Megaselia halterata, the ScP stain caused 56–83% reduction in L. mali populations whereas the SN strain caused 51–73% reduction. Two doses of the improved strain (0.5 times 10⁶ and 1.0 times 10⁶ infective juveniles per m² cropping area) did not differ in efficacy from diflubenzuron which caused 80% reduction in L. mali populations. The lower dose (0.5 times 10⁶) of the SN strain was less effective than diflubenzuron. The ScP strain had a major advantage over the SN strain in persistence in casing material. Nematodes had no significant effect on mushroom yields.     

Influence of Steinernema feltiae and Diflubenzuron on Yield and Economics of the Cultivated Mushroom Agaricus bisporus in Dutch Mushroom Culture

The insect pathogenic nematode Steinernema feltiae (Nematoda: Steinernematidae) was shown to offer an alternative to the use of diflubenzuron for the control of the mushroom fly Lycoriella auripila (Diptera: Sciaridae). The influence of diflubenzuron and S. feltiae treatments on the yield and numbers of the mushroom, Agaricus bisporus , was studied. Applications of diflubenzuron after casing significantly reduced total mushroom yields by 10-13%. The greatest yield reductions were observed in the first flush. In the second flush, high yields were found despite significantly lower numbers of mushrooms. These high yields, however, could not compensate for the yield loss of the first flush. Some of the treatments with S. feltiae significantly increased yields, but these were not associated with a particular time of application. As nematodes did not reduce mushroom yields they were able to compete with diflubenzuron. Although the purchase costs of nematodes were high, their use was more economical than that of diflubenzuron when the yield losses of 10% due to casing treatments were taken into account.     

Effects of bendiocarb and diflubenzuron on mushroom cropping

When mixed into the casing or compost layers of a mushroom bed in the absence of pests, bendiocarb decreased yield and number of mushrooms according to concentration. The most severe effects were on mushroom number at the two highest rates used (100 and 1000 μg/g), and there were large increases in mushroom size. Effects of bendiocarb incorporation in the compost diminished with time, and there was partial compensation in yield and numbers at the fourth flush. The action of bendiocarb persisted when it was mixed into the casing. Diflubenzuron showed some opposite effects at lower concentrations. When either mixed into, or drenched onto the casing at the commercial rate (30 μg/g), yield and size were both increased and the timing of the flushes was unaffected. At the two higher concentrations (180 and 1080 μg/g), reductions in yield and number and an increase in mushroom size were shown. However, these effects became more severe with time, especially those on mushroom number, possibly due to the accumulation of a toxic breakdown product.     

Laboratory rearing, biology and chemical control of the mushroom sciarid Lycoriella auripila (Diptera: Lycoriidae)

The mushroom sciarid was found to develop on a plant-derived diet of oat or soya meal. Details of simple rearing techniques and insecticidal assays of treated casing are given. In laboratory tests using ten chemicals, chlorfenvinphos and pirimiphosethyl showed persistent activity against larvae when used at 15 ppm and are suggested as suitable for incorporation in peat-chalk casing mixtures to give protection throughout cropping. The low figures obtained for phytotoxicity and residues in the crop suggest this technique would be acceptable in commerce. Diazinon remained active in casing for only a short time.     

Pseudomonas tolaasi in Mushroom Crops: A Note on Primary and Secondary Sources of the Bacterium on a Commercial Farm in England

Primary sources of Pseudomonas tolaasi Paine on a mushroom farm were the peat and limestone used in the casing process. The pathogen could not be detected in the farm soil, water supply, the mushroom spawn used, or in compost after spawning, but was isolated from the casing (peat/limestone mixture) layer of symptom-free mushroom beds and both the casing layer and compost of beds bearing diseased mushrooms. Secondary sources were numerous once the pathogen was present in mushroom beds. These included symptomless and diseased mushrooms, the fingers and shoes of people handling the crop, their baskets, knives and ladders. Ps. tolaasi could be isolated from dust in the air in infected houses and also from floors. Spores of infected mushrooms may transport the bacterium, as did sciarid flies and mites which are common pests of mushroom crops.     

Effects of Application Rates of Steinernema feltiae (Nematoda: Steinernematidae) on Biological Control of the Mushroom Fly Lycoriella auripila (Diptera: Sciaridae)

The potential of Steinernema feltiae for the biological control of Lycoriella auripila was tested in commercial mushroom‐growing conditions. The nematodes, applied at rates of 1.5, 3, 6 or 12 x 10 ⁶ infective juveniles per 34 kg tray of spawn‐run compost, were mixed into the casing material before it was spread over the compost surface. When compared with untreated control trays, any rate of nematode application significantly reduced fly emergence. Insecticides significantly reduced mushroom yields; nematodes significantly increased them. At a rate of 3 x 10 ⁶ infectives/tray S. feltiae elicited mean total increases in the weight and numbers of mushrooms produced of 8% and 11% respectively. The nematodes also reduced the incidence of mushrooms spoiled by tunnelling sciarid larvae. The early decline in the numbers of nematodes persisting in casing was a trend that was reversed later, when evidence was obtained that S. feltiae was recycling in insects that had been killed. When applied at a rate of 3 ‐10⁶infectives/tray of compost S. feltiae should provide reliable and cost‐effective biological control of L. auripila.     

The effect of some microphagous saprobic nematodes on mushroom culture

When added to spawned mushroom compost the microphagous saprobic nematodes Pelodera cylindrica, Mesorhabditis spiculigera and Acrobeloides bütschlii did not affect mycelial growth or compost pH. The eelworms multiplied at first but their numbers declined as the mycelium colonized the compost. In contrast, the fungal-feeding Aphelenchoides composticola increased rapidly and destroyed the mycelium. Excess water, and the presence of the fungal competitor of mushroom, Chaetomium olivaceum, allowed some increase of the microphagous forms. Different numbers of Mesorhabditis spiculigera added to the ‘casing’ had no effect on mushroom yield but the mushroom ‘flushes’ seemed less pronounced. Reasons for the failure of the saprobic eelworms to affect mushroom, and the possibility of synergistic pathogenicity by these eelworms and bacteria, are discussed.     

Re-supplementing and re-casing mushroom (<Emphasis Type="Italic">Agaricus bisporus</Emphasis>) compost for a second crop

Experiments were performed to determine the effect of adding nutrient supplements to colonized mushroom compost (MC) for the production of a second crop of mushrooms. Mushrooms were harvested for 1, 2 or 3 flushes, the casing removed and the MC then was fragmented and re-supplemented with delayed release supplements treated or non-treated with fungicide (thiophanate-methyl; Topsin M 70WP) and re-cased. Overall double-crop yields were higher when MC was re-supplemented after 1st flush (1st flush MC) as compared to re-supplementation after the 2nd or 3rd flushes. Mean double-crop BEs were 128, 119 and 109% when 1st-, 2nd- and 3rd-flush MCs were used, respectively. Treatment of delayed release supplement with thiophanate-methyl fungicide did not affect mushroom yields. Soluble salts and potassium concentrations increased 350 and 900%, respectively, in the casing overlay through three flushes suggesting that removal of the casing would help to alleviate the build up of these potential growth-limiting materials. Re-supplementing and re-casing of MC represents a potential opportunity for growers to increase revenues and reduce costs associated with preparation and disposal of compost. The ability to double-crop mushroom compost would provide growers a chance to increase yields by 40% or more, depending on whether they re-supplement and re-case after 1st, 2nd or 3rd flush.     

Substrate dependent larval development and emergence of the mushroom pests Lycoriella auripila and Megaselia halterata

Pasteurized, spawned, full-grown and immediately-cased full-grown compost were simultaneously exposed to natural populations of the mushroom pests Lycoriella auripila (Winnertz) (Diptera: Sciaridae) and Megaselia halterata (Wood) (Diptera: Phoridae). Different numbers of adults emerged from each of these composts. Highest numbers of L. auripila emerged from spawned and pasteurized compost whereas lowest numbers of L. auripila emerged from full-grown compost. the emergence from full-grown compost was delayed, which could be explained by the delayed development of the larvae in this type of compost. High numbers of M. halterata emerged from compost that was completely colonized by the mycelia of the edible white button mushroom Agaricus bisporus (Lange) Imbach. The immediate covering of the compost with a casing layer significantly lowered the numbers of emerging M. halterata flies. Compared with the emergence pattern from full-grown and immediately-cased full-grown compost, adult M. halterata showed a delayed pattern of emergence in spawned compost. Adult M. halterata did not emerge from pasteurized compost. The results of these experiments enabled us to improve the timing of the application of insect pathogenic nematodes in the control of the larvae of both insect pests.     

Laboratory evaluation of cyromazine against insecticide-resistant field strains of Musca domestica

A screening programme was undertaken to examine the possibility of cross resistance occurring between cyromazine and conventional insecticides. The responses of nine strains of Musca domestica to treatment with cyromazine, trichlorphon, methomyl and pyrethrins with piperonyl butoxide were measured. No tolerance to cyromazine was found, neither was there a direct correlation between larval responses to cyromazine and adult responses to other insecticides. Cyromazine is a potent larvicide against M. domestica and the results of these tests show that it has good potential for the control of houseflies with high levels of resistance to other insecticides.     

Life table of Gaeolaelaps aculeifer (Acari: Laelapidae) feeding on larvae of Lycoriella auripila (Diptera: Sciaridae) with stage-specific estimates of consumption

Gaeolaelaps aculeifer (Canestrini, 1883) is a soil-dwelling predatory mite with potential for use as a biological control agent of fungus gnats (Diptera: Sciaridae) in mushroom production. The life table, predation rate and population growth rate of G. aculeifer on a diet of larvae of the sciarid fly, Lycoriella auripila, at 23?±?1°C, 60?±?5% RH and a photoperiod of 0:24 (L:D)?h was investigated. The results revealed that the duration of egg, larva, protonymph, deutonymph, females and males of G. aculeifer were 3.8?±?0.1, 1.4?±?0.1, 3.9?±?0.1, 4.1?±?0.1, 67.7?±?2.8 and 60.3?±?3.1 days, respectively. Net reproductive rate (R₀) was 54.8?±?7.1 offspring, intrinsic rate of increase (r) was 0.12?±?0.01 offspring day^?1, finite rate of increase (λ) was 1.13?±?0.01 day^?1and mean generation time (T) was 32.3?±?0.6 days. The predator consumed a mean of 0.08?±?0.05, 1.73?±?0.18, 3.16?±?0.28 and 75.9?±?7.1 third instar L. auripila larvae during the larval (1.3?±?0.1 days), protonymph (3.9?±?0.1 days), deutonymph (4.1?±?0.1 days) and adult (52.6?±?2.2 days) stages. Population parameters and consumption rates suggest that G. aculeifer has good potential as a biological control agent of L. auripila in mushroom production.     

Control of mushroom sciarid fly Lycoriella ingenua populations with insect growth regulators applied by soil drench

Mushroom sciarid fly Lycoriella ingenua (Dufour, 1839) comb. nov., is one of the most common fly pests affecting the cultivation of Agaricus bisporus (Lange) Imbach in Turkey. In this study, eight insect growth regulators (IGRs)--diflubenzuron, flufenoxuron, lufenuron, methoprene, novaluron, pyriproxyfen, teflubenzuron, and triflumuron-were tested for their potential to control L. ingenua populations in two successive growing periods. Treatments were targeted at larvae as soil drenches; treatment efficacy was evaluated by assessing adult emergence and larval damage. These products were compared with a control treated with water (negative control) and a conventional chemical insecticide (chlorpyrifos ethyl) (positive control). Treatments with the IGRs caused significant reductions in emerging adult numbers and sporophore damage rates compared with the water-treated control over the two growing periods. Of the IGRs tested, novaluron, diflubenzuron, and teflubenzuron had significantly lower numbers of emerging adults than the rest of the IGRs and chlorpyrifos ethyl-treated control in both periods. Treatments with teflubenzuron, pyriproxyfen, novaluron, and diflubenzuron resulted in significantly lower sporophore damage rates than all other treatments. Compared with negative control, there were no significant yield reductions due to applications of selected IGRs. The results suggest that all the IGRs tested can be used as alternatives to conventional pesticides in controlling L. ingenua populations on mushroom.