P ENNSYLVANIA Mushroom Integrated Pest Management

H andbook The PA IPM Program is a collaboration between the

Pennsylvania Department of

Agriculture and The

Pennsylvania State University College of Agricultural aimed at promoting Sciences

Integrated Pest Management in both agricultural and nonagricultural settings.

This publication was developed by the PA IPM program with the cooperation of the American Mushroom Institute. Table of Contents

Introduction 4 I. Theory of Integrated Pest II. Integrated Pest Manage- P. Coles Management 5 ment in Mushroom Production 20 A. History, Definitions, and the Economic Threshold 6 A. Specific Control Techniques S. Fleischer 1. Exclusion 21 B. Pesticides and Resistance in P. Coles IPM 13 S. Fleischer 2. Cultural Control 27 P. Coles/W. Barber 3. Biological Control 33 D. Rinker 4. Chemical Control 37 P. Coles B. Pesticide Safety 43 S. Whitney C. Pest Species Biology and Control 1. Arthropod Pests 47 C. Keil 2. Fungal Pathogens 52 P. Coles/W. Barber 3. Weed and Indicator Molds 61 D. Beyer 4. Bacterial Diseases 75 P. Wuest 5. Nematodes 78 P. Coles 6. Virus Disease 85 P. Romaine Introduction In this handbook we have addressed the Mushroom growing lends itself natu- Other features of mushroom production most important pest organisms with the rally to IPM. It is one of the few forms make IPM a necessity, not an option. potential to reduce mushroom yield and of agriculture in which the crop is With production measured in pounds quality. The handbook is intended for grown inside climate-controlled per square foot rather than in bushels or growers, as well as researchers, as both buildings. This offers two advantages tons per acre, mushroom growing is an educational tool and a reference not available to most other crops. First, very dense farming. If a pest gets into a manual. Recommendations presented control of the internal environment of room, it can spread rapidly because of here are not intended to bind growers in the growing room provides an impor- the large amount of food available their decision-making processes. Rather, tant weapon against many pests. within a relatively small space. In they should serve as a guide for develop- Temperature and humidity manipula- addition, many pests cannot be con- ing effective Integrated Pest Manage- tions, for instance, are two of many trolled using chemical pesticides, either ment (IPM) programs. Each grower cultural options available in mushroom because there are no products labeled should develop specific operating pest control with IPM. Second, since for mushroom use, or because materials procedures and checklists specifically the crop is grown indoors, pests can be don’t even exist for a specific type of tailored for individual use. In addition, excluded. This control measure is pest organism. Increased regulations are as technology is always changing, this unavailable to farmers of field crops, driving up the cost of producing new handbook will be updated periodically. who have little control over pest pesticides, making it difficult or invasion. An effective IPM program impossible for chemical manufacturers The handbook is divided into two parts, takes advantage of these particular to invest in a minor-use crop like covering the theory of IPM and the characteristics of mushroom growing. mushrooms. Usually, we are forced to practical aspects of IPM in mushroom rely on pesticides developed for other growing. The theory section defines commodities. An IPM program that IPM and gives it historical perspective. excludes pests and takes advantage of It also explains the concepts of pest the ability to manipulate the growing management and types of control, and environment not only is a more effective the importance of understanding pest means of pest control but also allows life cycles and biology. The section on limited dependency on chemical IPM in mushroom growing describes pesticides. how unique features of mushroom crops can be used effectively in IPM, and how These features make the IPM approach the theory of IPM can be applied the most effective and economical effectively. means of long-term sustainable pest control. Anyone trying to control pests without IPM eventually will end up at the mercy of those arthropods and mushroom diseases. We hope this manual will help you avoid that fate.

4 I. Theory of Integrated Pest Management

5 A. History, Definitions, and the Economic Threshold

Shelby J. Fleischer

These efforts at supervised control Integrated pest manage- History, Definitions, and declined rapidly when DDT and other the Economic Threshold new insecticides came into use. By the ment is the [information- late 1940s, over 90 percent of acreage Vernon M. Stern was working for the was treated with new materials, calcium based] selection, integra- Westside Alfalfa Pest Control Associa- arsenate fell into disuse, and the Pest tion in the San Joaquin Valley, Califor- Control Associations disappeared. The tion, and implementation of nia, a big association of growers new materials worked well for less cost, involving 10,285 acres when it formed so Vernon M. Stern went to graduate pest control based on in 1945. The association was organized school with Ken Hagen, the first person to help decide when to apply insecti- in charge of the Westside Association, and Robert van den Bosch, who had predicted economic, eco- cides against the alfalfa butterfly. also been in charge of the Association The alfalfa butterfly was not the most for a period of time. They worked with logical and sociological serious pest in alfalfa, but at times it Professor Ray F. Smith, who had flared up and caused very serious loss. initially organized the Pest Control consequences. Alfalfa growers had materials like Associations. calcium arsenate at their disposal, and they used these materials frequently, but It was not long before another insect, at significant expense and with hard the spotted alfalfa aphid, came into the Bottrell, 1979. work. The growers formed an associa- San Joaquin Valley, and by 1955 this tion after entomologists showed that a aphid was resistant to pesticides. Smith and his students (Stern, van den Bosch, Council of Environmental parasitoid controlled the butterfly most of the time, and that growers could and Hagen) imported an exotic parasi- Quality make many fewer pesticide applications toid and studied native predatory if they could estimate how well the insects. Both the parasitoid and the parasitoid was controlling the butterfly predators were effective when not larvae early in the crop growth cycle. destroyed by pesticides. They then The association hired people to do the found insecticide materials and use fieldwork and calculations and to give patterns that were relatively selective, advice. The Westside Alfalfa Pest allowing the natural enemies to coexist Control Association called this “super- with the valuable insecticide tools. vised control.” The system was success- ful, and soon the Westley Pest Control Association and the Tracey Pest Control Association formed in other parts of California.

6 In 1959 Vernon M. Stern with his co- The concept of economic injury level is This “Integrated Control” concept, authors Smith, van den Bosch, and shown in Figure 1. (Similar figures can published in 1959, was quickly ex- Hagen, wrote a paper entitled “The be found in Stern’s paper, published panded to include all methods of Integrated Control Concept,” (Stern et about 40 years ago, and similar concepts control. Thus, the Integrated Pest al. 1959) in which they generalized were in use in cotton production almost Management concept was born at least about integrating biological controls 75 years ago.) The figure shows that the 40 years ago. The concept was not born and insecticides. To make this work, pest density is changing over time. At solely in California; similar develop- they discussed monitoring, which low densities, the costs of the damage ments were occurring in Arkansas for requires understanding of sampling and done by the pests are less than the costs cotton crops and in Canada for apples. measurement of pest density. They of control, so it does not pay for the The concept arose from a philosophy noted how pest populations fluctuate manager to add the control. At higher for which the objective is to manage a over time. By monitoring density, they densities, however, it does pay to pest population below economically argued, intervention with pesticides can control. Pest density is dynamic, and damaging levels, and in a way that is be limited. This practice limits chemical managers can make short-term predic- practical for growers, by integrating applications to those necessary times tions about what the density soon will multiple control options (see Perkins and places where other tactics are not become. Managers usually want or need 1982 for a full historical perspective). sufficient. to implement controls a short time IPM always has emphasized integration before the Economic Injury Level is of control tactics, including pesticides, So when does it become necessary to reached. The Economic Threshold is the and monitoring to help determine time intervene with pesticides? In many density at which controls are added. It is and location for pesticide application. respects, this is an economic decision. It set so that, if controls are applied and requires relating economics or commer- are effective, the Economic Injury Level cial goals of production to fluctuating is not reached. pest density. Simply defined, the time to intervene with a pesticide is when the Figure 1. Graph of economic injury level. expected gain from using the pesticide equals the costs associated with its use. Pays to Control The pest density at which the gain equals the cost is the Economic Injury Level. Thus, IPM relates pest popula- tion dynamics to commercial produc- Pest Population tion goals.

Economic Injury Level

Does Not Pay to Control

Time

7 Today, there are many definitions of Integrated Pest Management. They all Problems With Pesticide Overuse recognize that many factors influence pest dynamics, the way these dynamics Over time, well-documented problems with sole or over-reliance on pesticides relate to production agriculture, and the were discovered, and they still are being discovered. Use patterns, rates, timing, need to integrate multiple control and other aspects of pesticide application are designed to minimize these strategies to manage pests over a long problems. Pesticides are an important part of IPM, but not the only part, and time frame. IPM has foundations in they require a good understanding to be used well. To ensure safety and conduct ecology—an understanding of the business legally, it is essential to follow the label and to realize that changes to relationships of the pest and beneficial labels occur frequently. Information for pesticide use is printed on the label, organisms within the biotic and abiotic which is a legal document, and must remain with the pesticide container. Over- environment, and an understanding of reliance on pesticides has been linked to problems, including: the distribution and abundance of these organisms. IPM emphasizes creating Resistance conditions to preclude an organism A change in the genetics of the pest population that impairs control in the field. from reaching pest status, correctly Depletion of natural controls diagnosing and monitoring pest Mortality of predators or parasitoids, which results in pests reaching even higher pressure, and allowing natural mortality densities (called resurgence) or species that were not previously pests reaching factors to work as well as possible. IPM pest status (called secondary outbreak). is a philosophy, a way of thinking, an attitude, which is adapted in practice to Biomagnification meet economic realities of commercial A build-up of the pesticide in fatty tissue, followed by an increase in the concen- production and modified as those tration of the pesticide in organisms higher on the food chain, including realities or tools available for manage- humans. ment change. A slightly modified definition of IPM from the Council of Environmental contamination Environmental Quality is “. . . the Unacceptable levels of the pesticide in groundwater, or in parts of the environ- [information-based] selection, integra- ment where pesticides were never meant to be. tion, and implementation of pest Species displacement control based on predicted economic, A change in the biodiversity of an area caused by the effect of pesticides on ecological and sociological conse- species populations. quences” (Botrell 1979).

Endocrine disruption Pesticide (and other) molecules acting upon the hormonal system of animals and humans, affecting their development and immunological processes.

Human health danger Direct or chronic toxicity to applicators or manufacturers; or to consumers caused by unacceptable residues in food.

8 We easily can recognize an IPM Sanitation An IPM Philosophy in philosophy in past and current manage- Here’s where mushroom growers can Mushroom Production ment of pests in mushroom production. excel compared to many other agricul- Management tactics are related to the tural production systems. The con- IPM in mushroom production got its biology and ecology of pest species and trolled environment required for start when sciarid fly populations began the relationship of the pests to yield, mushroom production allows for use of to explode in the late seventies as the quality, or marketability of the crop. steam-pasteurization at the beginning result of environmental changes brought There are a variety of tools in mush- and end of the crop, and sanitation of on by the availability of air condition- room production that influence pest the growing rooms and equipment. ing. Before air conditioning, mush- density and dynamics. These are not Biological control rooms were produced only in the cool mutually exclusive, and are best inte- Influencing the density or activity of season. When crops were most suscep- grated so that one tactic helps another. beneficial organisms, either through tible to infestation, it was usually too Many specific strategies with specific pests are discussed in the following cultural management or inundative cold outside for wild populations to be chapters, but it is worth pausing to release of additional beneficials into the mobile, thus they were not able to enter consider general terms that classify environment. Composting techniques growing rooms. Also, the summer was a control strategies and their relevance to influence biological control of fungi. break in the growing cycle, and thus mushroom production: Purposeful release of Pteromalid also a break in the life cycle of sciarid parasitoids on the composting wharf, or flies within mushroom houses. Exclusion entomopathogenic nematodes, are Techniques that help prevent the pest With the advent of air conditioning, examples of inundative release of from reaching sites where it can create there was no longer a break in the beneficials used in mushroom produc- damage, such as sealing walls and growing cycle, and sciarid flies were able tion. cracks, to prevent entry of flies. Air to breed uncontrollably. Despite the use must be filtered before it enters the Chemical control of chemical pesticides, the flies were rooms. Any personnel or equipment Introducing chemicals to kill pests. The winning the battle. By the summer of entering a room must be clean and/or types of chemical tools available are 1978, fly populations in Chester and sanitized. changing rapidly, and mushroom Berks Counties in Pennsylvania were growers have kept up with this change. causing severe crop loss. Delaying access Compare, for example, the types of Techniques that slow the rate at which a The Pennsylvania State University materials listed in Duffy 1981 with pest reaches sites where it can create Fleischer and Keil 1994. The 1970s began an interdepartmental Integrated damage. Examples include maintaining relied on broad-spectrum materials that Pest Management program for the sanitation in the premises around had activity against a wide range of mushroom industry in early 1979. The mushroom growing houses and keeping insects; the 1990s relied more on insect goal of the program was to reduce pest grass cut and trees trimmed. populations in an ecological way to growth regulators that have much economically tolerable levels. The Cultural control greater selectivity and are more precise program was to study four major Growing techniques that make the in what they target. This trend of mushroom pests and diseases: the environment less supportive of pests greater selectivity can be expected to sciarid fly, Lycoriella mali (Fitch); the and more supportive of beneficial continue. In an IPM program, these phorid fly, Megaselia halterata (Wood); organisms. Composting is an excellent chemical tools are used in a way that is Verticillium or dry bubble, Verticillium cultural IPM technique that strongly as compatible as possible with the other malthousei; and bacterial blotch, influences fungal competitors and tools listed above, as well as with Pseudomonas tolaasi. The most impor- pathogens. Instigation of shorter crop pesticide resistance management, which tant components of the program were cycles is another IPM tool that strongly is discussed later in this chapter. monitoring and identifying pests and influences pest population dynamics. diseases. Mushroom pest adults as well Also important is maintaining an as larvae and eggs were monitored and environment, including proper tem- identified, and mushroom beds were perature and relative humidity, that sampled for diseases so their life cycles favors mushroom growth over its could be studied. competitors’.

9 Biorational materials peratures are monitored in both Phase I determines whether or not a pesticide or Synthesized or extracted compounds and II. Though this is not a direct other management strategy is working that are applied to manage pest densi- measure of populations, it is a good and calls attention to times when ties, which often have much greater indicator of what is happening strategies are not working as expected. selectivity upon target pests. Examples microbially; if the compost is cold near Sometimes pest pressure increases after a used in mushroom production include the center of the pile—for example, pesticide is applied. Perhaps new insect growth regulators, botanical 120°F (49°C)—it is an indication that immigrants arrived, or they arrived extracts, and microbial metabolites. there are anaerobic organisms producing more quickly than anticipated, or a the wrong type of compounds. This is stage of the pest that was not susceptible Clearly, mushroom growers can and do not a direct measure, but it is very to the pesticide developed into a stage integrate multiple control strategies, as important to the quality of the compost that is now a problem. Perhaps the pest in an IPM program. Further, there is and reminds the growers that the population is developing resistance to the issue of relating decisions to pest compost is alive, something that usually the pesticide currently in use. Clearly, population dynamics: the Economic gets very little attention. monitoring is an essential part of IPM. Injury Level or Economic Threshold. The level of pest density that can be Rules of thumb provide economic It is clear that the philosophy of IPM is tolerated is both a management and injury levels for some pests. For ex- compatible with mushroom production. subjective decision. Not every farm is ample, fly pressure may be low enough The Penn State Handbook for Commer- the same. Both the gain achieved by the during the winter to not require cial Mushroom Growers (Wuest 1992) is use of the material and the market price insecticides. An economic injury level of filled with valuable information about of the mushrooms will vary among adult sciarid counts per day, as deter- identification, diagnosis, cultural farms and through the season on a given mined on the Pennsylvania Mushroom controls, monitoring, and management. farm. Economic goals also vary: some Fly Monitor, is shown in Figure 3. In A basic premise is that no single control farms may emphasize quality factors for this example, there is virtually no method will be successful over time. select markets, others may emphasize tolerance for flies before, and 3 days IPM strives to integrate control tactics, volume. after, spawning. After spawning, the which essentially are different types of threshold rises to ten flies per strip per technologies. IPM will use cultural and In addition, other biological factors day. The threshold rises again slightly biological tactics to the best degree should influence management decisions soon after casing and more dramatically possible and then include pesticides as about the tolerable levels of a pest. For at pinning. The idea is that flies arriving needed. Control technologies discussed example, if sciarid flies are aiding early will cause greater damage and are a in this publication include Diagnosis transmission of a pathogen or mites, sign of much greater problems that will and Monitoring, Exclusion (Chapter then the tolerable pest density of flies occur before the crop is complete, but II.A.1), Cultural Controls (Chapter should drop dramatically. The tolerable flies arriving later will have less opportu- II.A.2), Biological Controls (Chapter pest density is also different at different nity to cause damage because they have II.A.3), and Chemical Controls (Chap- times in the crop growth cycle. This less time to complete another life cycle. ter II.A.4). tolerable pest density is best developed This specific threshold may not be the through experience and in consultation best for your facility, as the cropping Technologies change over time. What with others who have had growing cycle and other factors may not be mushroom growers may not realize is experience. exactly the same, but it does demon- that they can be among the best at strate that thresholds can influence adapting to these changes. Changes in In an IPM philosophy, growers do not technology are true for cultural tech- strive to remove every individual pest at management and suggests that thresh- olds can be adapted to your farm. nologies as well as for biological and every moment. Rather, management pesticide technologies. Consider the involves monitoring pest pressure and Monitoring is essential for defining change in growing technology, varieties, using that information to influence when and where to invest pest manage- and cropping cycles over the last 20 management. In mushrooms, monitor- ment inputs. The first step in monitor- years. Because the technologies keep ing includes fly monitors and record ing is identifying the pest and diagnos- changing, the IPM program also must sheets (Figure 2), nuisance fly monitors ing the problem. Monitoring also is adapt, change, and improve. It is clear on the composting wharf, and routine essential for evaluation and follow-up. It that the IPM philosophy of integrating inspection of beds for diseases. Tem-

10 Figure 2. Pennsylvania mushroom fly monitor record sheet.

Pennsylvania Mushroom Fly Monitor Records

Block Number: Room Number:

Number and Number and Day Date Name of Flies Day Date Name of Flies

-6 +8

-5 +9

-4 +10

-3 +11

-2 +12

-1 +13

Spawning +14

+1 +15

+2 +16

+3 +17

+4 +18

+5 +19

+6 +20

+7 +21

Cecid Fly Phorid Fly Sciarid Fly

Instructions for use: Record daily fly counts from the monitor for days -6 thru +21 from spawning. Note whether the flies are cecid (=C), phorid (=P), or sciarid (=S).

Note: A 10x hand lens will be helpful in insect identification.

11 Figure 3. Pennsylvania mushroom fly monitor action levels. Adult sciarid fly counts determine the need for insecticide applications in a growing room. Selected References 20 Bottrell, D. R., Council on Environ- mental Quality. 1979. Integrated Pest Management. U.S. Government 10 Printing Office 286-007/6007.

Duffy, M. D. 1981. Mushroom Inte- grated Pest Management and the Cost of

Number of Insects per Strip Insects per Number of Current Management Techniques. M.S. 0 -3 -1 1 3 5 7 9 11 13 15 17 19 21 Days Thesis. The Pennsylvania State Univer- ▲ ▲ ▲ sity. Spawning Casing Pins Fleischer, S. J. and C. B. O. Keil. 1994. multiple management tactics and available, and IPM is a philosophy that Insecticide priorities in the U.S. allowing pest density dynamics to can integrate and prioritize these mushroom industry. Mushroom News influence management is well embed- options. Fundamentally, an IPM 42: 7–10. ded in the modern mushroom farm. program identifies and monitors the Perkins, J. H. 1982. Insects, experts, and pest, takes advantage of the options that In subsequent chapters, note how often the insecticide crisis. The quest for new manage the pest through cultural a range of management options are pest management strategies. Plenum means, and adds pesticides when discussed and how these options require Press. New York. 304 pp. needed. The new pesticides will bring an understanding of the life cycle of the improved safety and environmental Stern, V. M., R. F. Smith, R. van den pest and an understanding of how the profiles. To be preserved, they should be Bosch, and K. S. Hagen. 1959. The pest interacts with the biotic and abiotic implemented in conjunction with a integrated control concept. Hilgardia environment (in other words, the pesticide resistance management 29: 81–100. ecology of the organism). In the future, program. new technological options will become Wuest, P. J. (ed). 1992. Penn State Handbook for Commercial Mushroom Growers. The Pennsylvania State University.

12 B. Pesticides and Resistance in IPM

Shelby J. Fleischer

Changes in technology are easy to see. pesticide during the last 40 years What may not be as obvious is that the (Georghiou and Taylor 1986). The pests themselves keep changing. Perhaps increase in numbers of resistant species the most important change is the has been exponential for these last 40 development of resistance. In many years. More recently, the increase in agricultural systems, resistance has been resistant populations of pathogens and the single most important factor causing weeds are beginning to follow the same the decline of a pest management curve. It should come as no surprise, strategy. therefore, that resistance in mushroom pests is now well documented. Ex- Resistance is a genetic change, occurring amples include sciarid flies, which are in response to selection by toxicants, resistant to pyrethroids (Keil and that may impair control in the field. Bartlett 1996); house flies and stable Pests can withstand toxins to some flies on the composting wharf, which degree, often in relation to the dose to are resistant to many classes of insecti- which they are subjected. There is cides; and verticillium, which is resistant variation in this ability to detoxify; that to benomyl. is, some individuals can detoxify more easily than others. Pesticides are one Resistance must be evaluated with type of toxin, and when they are respect to the natural variation among applied, individuals in a population are individuals and populations in their killed. If individuals with improved abilities to detoxify a pesticide. It can be ways to detoxify exist, selection for a matter of opinion as to when to label a those individuals will inadvertently population as resistant, and when it is occur. They will survive and reproduce just displaying natural variation. The more easily than other indiviuals in an World Health Organization has set a environment that includes the pesticide. standard of 10; that is, when a popula- This process is known as selection for tion requires 10 times the amount of resistant individuals by the toxicant. pesticide to kill 50 percent of a test Continued selection will result in a population compared to a reference resistant population. This is evolution in susceptible population, it is classified as action, and it is the same process that resistant. Also, it is very common for results in strains of human pathogens populations to exhibit different abilities becoming resistant to antibiotics. to withstand pesticides in different geographic areas. Thus, a pest may be Evolution of resistant pest populations resistant in only certain, often small, is a common fact of agriculture today. geographic areas. With this in mind, it Over 500 pest insect species have also is possible to recognize limited evolved resistance to at least one resistance of sciarids to diflubenzuron.

13 Mutations cause the variation of DNA example, one in 1,000 individuals now Resistance Management among individuals. Mutations are rare would be surviving the pesticide (perhaps one in a million at a given treatment. That represents a 100-fold The realistic potential for resistance is a site), but they are present. For example, increase in the frequency of resistant predictable, evolutionary consequence if mutations occur at a rate of one in a individuals! The key to effective of pesticide use (and other management million at a given site on a long strand resistance management is to start a tactics as well). Therefore, resistance of DNA, and there are 100 million such resistance management program early. management is now considered and sites in the DNA of a human, then Do not wait until field failures become must be a part of integrated pest there are about 100 mutations occurring obvious; by that time, a dramatic management. As a new management in each human. In DNA, which codes increase in the frequency of resistant tactic such as a new chemical is de- for protein, mutations result in different alleles has already occurred. The best ployed, it should be used in a manner versions of the same protein. Most time to design a resistance management that is designed to prevent or slow the mutations have either no effect or are program is before a new product is ever development of resistance. This is harmful. Some, however, produce used. beneficial results; some proteins provide becoming especially important as we Crop protection companies are antici- move to the use of newer, selective individuals with improved abilities to survive and/or reproduce. pating the evolution of resistance to materials. The goals of resistance their new materials and are providing management are to avoid resistance, resistance management programs as part slow the rate of resistance development, Principles of Resistance of the initial introduction of a new and cause resistant populations to revert Management material. In some cases, companies are to more susceptible populations. monitoring for resistant alleles at the To best understand resistance manage- When a pesticide with a new mode of time of introduction, with sensitivity ment, it is helpful to understand the action is introduced into commercial that would detect the very low levels details of the evolutionary process that use and gains acceptance, it can be expected in the early stages of resistance results in resistance. When measuring assumed that it is effective. At that development. Pesticide Resistance something about an individual, such as point, it kills the target pest, and Management (PRM) is becoming a part its ability to withstand a pesticide, you resistance is not a problem. What has of IPM. are describing its phenotype. When been learned from many experiences measuring phenotypes for a population with pests that have evolved resistance is of individuals, the phenotype of that that alleles (segments of DNA that code population can be described (for for protein) that confer resistance are example, you may observe that 20 either not present or are present at very percent of a population withstands a low frequencies when the new material specific dose of a specific pesticide). first is used. These low frequencies are With resistance, we observe reduced often lower than can be measured rates of mortality (lower efficacy) when economically. For the purposes of this a pesticide is applied. exercise, assume that resistant alleles are present in less than one in 100,000 Lower efficacy can be due to many individuals. causes. In fact, in most cases in agricul- tural settings, lower efficacy is caused by When this same pesticide is observed by application, timing, or something that is a grower to be not as effective as it used not related to resistance. However, when to be, and assuming that everything else lower efficacy is caused by a change in is the same, then resistance is probably the proportion of the pest population occurring. By that time, enough that carries a heritable genetic compo- individuals are carrying resistant alleles nent such as DNA, then lower efficacy to make it visible to a grower. For this to is due to resistance. happen, the resistant individuals would have to occur reasonably frequently; for

14 exceptions are important because they RR with RR to give RR Factors Affecting lead to stable resistance. However, in the Resistance Management RR with RS to give RR and RS presence of the pesticide, the R allele confers an advantage to individuals that The development and rate of resistance RR with SS to give RS contain it. Over time, the R allele is are affected by genetic factors, biological balanced with other alleles so that it RS with RS to give RR, RS, and SS and ecological factors, and operational may no longer be deleterious. factors-activities performed within and SS with RS to give SS and RS Biological and ecological factors refer to surrounding a production facility the biology and ecology of the pest. (Georghiou and Taylor 1986). SS with SS to give SS Reviews of the many pest species that Genetic factors refer to the genetics of have evolved resistance have shown some clear patterns. One important the pest itself. Does the capacity for When a pesticide is introduced into example is generation time. Pests that resistance exist? Do some individuals in effective commercial use, pest individu- quickly speed through one generation the population have alleles that code for als are almost entirely of the SS type. As after another have a much greater proteins that confer resistance? Do some resistance develops, some RS become potential of evolving resistance in detoxification proteins of some indi- present (from one in 100 to one in response to selection by pesticides than viduals work faster? Do some have 10,000), and there are many, many pests with slower generation times. thicker cuticles that slow the rate of fewer RR (from one in 10,000 to one in Similarly, pests that have a high repro- pesticide entry? Genetic factors vary— 100,000,000). Even if R alleles are ductive potential—each female generat- pests do have mutations—and it is present, it is desirable to keep many SS ing many offspring that survive long possible, although rare, that a new individuals nearby and mating, slowing enough to reproduce—evolve resistance mutation will confer resistance. For resistance development. So if the quicker. Immigration traits also are purposes of long-term resistance population can be swamped with important, but tend to work in the management, it should be assumed that, susceptible individuals, resistance can be opposite direction. Pest species that at some level, resistant alleles are slowed. This is important, because most have higher rates of immigration tend to present. For the purpose of the follow- of the population (say, from outside the have slower rates of resistance, because ing illustration, we will indicate resistant mushroom house) consists of suscep- the constant flow of S alleles into the alleles, pieces of DNA that code for tible individuals (SS) during early stages population serves as a resistance proteins that confer resistance, with a of resistance. In the early stages of management tool. Those species with capital “R.” Susceptible alleles will be resistance, the very rare RR individual low rates of immigration have greater indicated with a capital “S.” Most insect might have a greater chance of drown- chances of RS or RR individuals mating pests have two copies of each allele, so ing or desiccating—or dying from any with each other, which rapidly increases they may be indicated by “RR,” “RS,” number of causes—than mating. After a resistance. or “SS.” pesticide application, some individuals So what is the frequency of resistant with R alleles may survive, but some The host range of the pest also has alleles—what is the percent of the with S alleles might also (they may have shown a trend. Pests that have popula- population that displays resistance? The been in a protected growth stage, like tions spread out among many hosts higher the frequency, the higher the rate the egg stage, and may not have been (polyphagy) tend towards lower rates of of development of resistance. The R affected). As long as we can keep the resistance than those that specialize on allele is mixing every time an insect frequency of R low, we have an effective one host. This is because there is a mates. If RR individuals mate with SS resistance management program. tendency for patches of pest populations to exist on untreated areas, or refuges, individuals, offspring will be RS, With few important exceptions, the R and susceptible individuals existing in helping to dilute the R allele. Possible allele probably is mildly deleterious. For untreated refuges serve to maintain S combinations include: example, it may mildly reduce fecun- alleles. Pests that have many matings dity, at least initially, in the absence of (polygamy) also tend toward lower rates the pesticide. The initial R frequency is of resistance, because there is less chance held in check by a balance between for RR individuals to occur. mutation and selection, although

15 Operational factors are under the When resistance occurs, the curve The dosage applied determines selection grower’s control. These include the changes. The measured points don’t for resistance. If the dosage applied is timing and dose of a pesticide, choice of match the line as well, suggesting high enough, SS, RS, and RR individu- materials, decisions about tank mixing, greater variability in the relationship; or als are killed, and no selection is taking and decisions about alternating prod- the curve shifts to the right or gets more place—an event that rarely happens in ucts. Dosage, or application rate, often shallow, predicting that mortality is the real world. Even when it is possible determines if an individual is susceptible lower at the same dose, like this: to apply such a high dose, the pesticide or resistant. At some very high dose will decay over time, and new pest level, every individual will be killed, and Figure 5. Dose-mortality curve with individuals that arrive (either from insecticide resistance. at some low dose level all individuals immigration or development from will survive, regardless of whether they another life stage such as an egg) are carry R or S alleles. Measurement of the then experiencing a reduced dose. relationship between dose and mortality When a dose kills some individuals but is a dose-mortality curve. The dose- Killed Percent mortality curve shows the proportion of allows others to survive, it is called a the population killed on the y-axis selective or discriminating dose. A dose against the dose on the x-axis. By that is able to separate genotypes (RR changing the way the numbers are from RS, or RS from SS), is a discrimi- 0.01 0.1 1.0 nating dose. This might occur when a represented, we can straighten out the Insecticide Dose or Concentration dose-mortality curve into a line. For a pesticide is applied to a mixed popula- single population, the curve looks like Thus, one way of monitoring for tion, or it might occur after a pesticide this: resistance is to plot the dose-mortality has been applied and is degrading into a relationship from different points in lower concentration. Figure 7 shows a Figure 4. Dose-mortality curve. time, or different geographic areas, or selective dose, where SS and RS different populations. Different popula- individuals are killed but RR individuals tions of SS, RS, or RR individuals will survive. result in different lines, like this: Figure 7. Dose-mortality curves for three populations, including selective Percent Killed Percent Figure 6. Dose-mortality curves for dose. three populations. Selective Dose Some killed, some survive

0.01 0.1 1.0 Insecticide Dose or Concentration

Percent Killed Percent

SS RS RR SS RS RR Killed Percent Susceptible Mix Resistant

0.01 0.1 1.0 0.01 0.1 1.0 Insecticide Dose or Concentration Insecticide Dose

16 In the example shown in Figure 7, the These examples also illustrate that the RS individuals are killed, but at a lower dominance of the R allele—whether Strategies and Tactics of dose. In the following example (Figure resistance is expressed in RS individu- Pesticide Resistance 8), selection might kill only SS indi- als—depends on the dose. When the Management viduals. This (Figure 8) is the worst-case dose is selecting for RR individuals and scenario for resistance management, killing RS individuals, the R allele is Applying the aforementioned theory to because there typically are more RS than recessive or not being expressed when it different strategies can help manage RR individuals. When the selection is is combined with the S allele. But when resistance. These strategies have been allowing RS individuals to survive, the the dose is selecting for both RR and RS classified as saturation, multiple attack, R allele will increase more rapidly individuals, the R allele is dominant. or moderation, and have been tested because there are more RS individuals. The effective or functional dominance with simulation models and limited varies under field conditions and field experiments in various agricultural Figure 8. Dose-mortality curves for depends on dose. three populations, including less- systems. effective selective dose. As can now be seen, population Saturation is an effort to prevent Selective Dose dynamics and population genetics Some killed, some survive selection by making sure even resistant interact. With resistance management, individuals are killed, typically with a the population of alleles (R and S) and high dose, and sometimes adding the population of individuals (the synergists to block detoxification. It has density of individuals of each type) been dubbed the “high dose, high risk” must be considered. For example, there strategy, and it works well if all pests are

Percent Killed Percent SS RS RR Susceptible Mix Resistant can be an unstable equilibrium, where R killed every time. To work, it needs to 0.01 0.1 1.0 is selected for but not maintained at be started while the initial R frequency Insecticide Dose high levels. This can occur within a is very low, and not after some concern large population where RR exists at a about efficacy is occurring. When pests low level. A discriminating dose selects re-invade, the saturation strategy works for the RR individuals, but there are few best when the immigrants are suscep- of them. If high rates of immigration tible individuals that mate randomly and mating of SS individuals follow, with the resistant ones, which is difficult most of the offspring will be SS and RS, to achieve in an environment of high although some RR will occur. Popula- dosage. The saturation model also works tion density, population genetics, and best on pests with a low reproductive resistance are fluctuating over time, and potential. Also, this strategy has high resistance management, as stated earlier, risk, because once it fails (when the dose is striving to avoid resistance, slow the is no longer killing all individuals but rate of resistance, or cause resistant allowing some RR, or even worse, some populations to revert to susceptible RS, to survive), it will continue to fail populations. quickly if it is not changed. It may be difficult on some mushroom farms to deliver and maintain a sufficiently high dose at all locations that need to be targeted. When using the saturation model, it is important to remember other concerns surrounding use of large amounts of pesticides.

The multiple attack strategy takes aim at different modes of action with rotations or tank-mixes of different materials. Rotations involve switching

17 materials for different applications and frequency of individuals resistant to Moderation strives to maintain suscep- require a good choice of material in the both materials is exceedingly rare. The tible individuals in the population using rotation. Ideally, any resistant individu- assumptions are that all individuals are all IPM tactics (cultural, exclusion, als surviving the first pesticide applica- susceptible to one or both materials, the mechanical, biological, etc.). Modera- tion are killed with the second material. materials decay at approximately equal tion attempts to preserve susceptibles in As in saturation methods, rotation rates, and as in rotation, there is no the environment and allow mating of works best when started very early, well cross-resistance. these SS individuals with those carrying before field failures are noted. This is the R allele. The goal is to keep the R because the few resistant survivors Cross-resistance refers to resistance that allele swamped with S alleles. Growers would have less chance of mating and developed against one material also should use application timing to try to producing offspring that also mate conferring resistance to another mate- preserve susceptibles early in the when their population is very low. rial. Cross-resistance has been fairly evolution of resistance, so that not every When populations are very low, lots of common for some insects and some pest individual is targeted at every natural mortality (drowning, desiccat- classes of modes of action. Cross- moment. Monitoring and timing ing, disease, etc.) can keep them low. resistance has occurred from one applications help preserve susceptibles. Issues about whether the R allele exists, pyrethroid to another pyrethroid, from Creation of refuges (refugia)—areas that and whether cross-resistance exists, the old organochlorines to the newer are not sprayed—also preserves should influence choice of material. To pyrethroids, and from organophos- susceptibles. Refugia can be in the work over a long time frame, rotation phates to carbamates. This is because mushroom house itself or in surround- assumes that the frequency of R to each there are some similarities in the modes ing habitat if they contribute to mating. material declines while it is not being of action of these materials at the used. This may occur when the next molecular level. To avoid cross-resis- In many studies, the decay rate of pest immigration is composed mostly of tance, choose materials with distinctly pesticides has strongly influenced the susceptibles (see below). Rotation also different modes of action. With rate of resistance, and fast-decaying assumes no cross-resistance. insecticides, current options include materials are associated with the insect growth regulators, pyrethroids, moderation management strategy. Tank-mixes also combine materials, but entomopathogenic nematodes, and Materials that decay quickly initially at the same time. They are sometimes protein crystals from Bacillus have a high (and hopefully non- used to help ensure efficacy. Some argue thuringiensis. There are new materials selective) dose, killing all genotypes. that tank-mixes also can be a resistance with yet other modes of action in the Then the fast-decaying materials are management tactic. Tank-mixes with pipeline as well, including microbial gone. There is little time during which materials of distinctly different modes of metabolites that affect GABA receptors, the dose is selective. Materials that action may help ensure that the second nicotinoid materials, botanicals, and decay slowly go through a longer time newer insect growth regulators that material kills the rare individual that is with a selective dose. In general, slow- target different parts of insect develop- resistant to one material. However, if a ment. Investment in research will help decaying materials—those often farm starts to tank-mix because a develop these materials for mushroom credited with “residual activity”—favor material is not working as well as before, production. All of these have very the development of resistance. They can it may be too late—the resistant different modes of action—some are exhibit selective activity over longer individual may not be so rare anymore. better classified as biological control times and make it harder for immigrat- Tank-mixes also add expense, and if materials, and their integrated use helps ing SS individuals to survive and mate problems arise, they are harder to make clear how pesticide resistance with the rare RR individuals that are diagnose. If the different materials do management is consistent with the surviving. Choosing materials with a not degrade in the same way, the pests philosophy underlying IPM. fast decay rate has worked as a resistance are not really exposed to both materials management tactic for house flies. at some time after the applications. In simulation models, tank-mixes work best when started early, while the R frequency for any material involved in the strategy is low, and when the

18 In most field examples to date, pesticide resistance management programs have Selected References required preservation and mating with susceptibles. Choice of short-residual Georghiou, G. P. and C. E. Taylor. materials has worked in models and in 1986. Factors influencing the evolution practice. Limiting application to specific of resistance. pp. 143–156 in National times of season or generations of the Research Council. Pesticide resistance. pest, or leaving refuges of untreated Strategies and tactics for management. areas with immigration of susceptibles National Academy Press. Washington, from those areas, have been useful and D.C. 471 pp. may require coordinated activities of neighboring growers. The most impor- Keil, C. B. O. and G. R. Bartlett. 1996. tant factors in simulation models Permethrin resistance in Lycoriella mali suggest that resistance is most influ- (Fitch) (Diptera: Sciaridae) on commer- enced by the reproductive potential of cial mushroom farms. Mushroom News the pest; also, that resistance is best 44: 8–13. slowed by immigration of susceptibles Roush, R. T. and B. E. Tabashnik, eds. and reduction of selection pressure by 1990. Pesticide Resistance in Arthropods. making applications only when needed, Chapman and Hall, New York. 303 pp. carefully choosing the dosage, and using shorter-residual materials. Taylor, C. E., F. Quaglia, and G. P. Georghiou. 1983. Evolution of resis- One take-home message is that mix- tance to insecticides: a case study on the tures, rotations, and saturation all influence of immigration and insecti- require conditions not well met in the cide decay rates. J. Econ. Entomol. 76: field; reducing pesticide use (via IPM) 704–707. has proven more productive than optimizing pesticide combinations and spatial deployments. Pesticide resistance management has relied on knowing pest biology and ecology, understanding evolution, and integrating management tactics. Technologies available for pest management are changing constantly to keep up with changing conditions for growing and marketing the crop and with changes in the pests themselves. A resistant pest population is a change in the pest population. Clearly, pesticide resistance management has a philo- sophical basis and is part of IPM.

19 II. Integrated Pest Management in Mushroom Production

20 A. Specific Control Techniques

Exclusion prevents the entrance of pest There are several ways to accomplish organisms into new rooms and their exclusion: the integrity of the building 1. Exclusion escape from older ones. The latter must be maintained; openings must be should not be underestimated. Pest secured (doors, fans for boiler or electric Phillip S. Coles populations usually are high in older rooms, etc.); air entering rooms must be rooms, and they threaten infestation of filtered; and the movement of people younger crops if they are not contained. and equipment must be restricted. Since mushrooms are grown inside environmentally controlled rooms, our Construction of new growing rooms industry is in a unique position in must permit easy sealing of the building agriculture: we are able to control pest and provide easy maintenance of that movement into and out of growing seal. All areas should have easy access. rooms. This must be exploited fully in Any areas not exposed for easy inspec- any mushroom IPM program. Once a tion can allow openings to form room is pasteurized successfully, pests undetected. Moldings along rooflines, will have to enter in order to become a for example, can hide cracks between problem. If exclusion were completely the wall and roof. Sometimes air successful, there would be no need for handling transitions or ducts are not any other form of pest control for most installed tight against the ceiling. The diseases. (Some organisms such as the space between the duct and ceiling can bacteria that cause blotch are not be so small that it is impossible to seal destroyed by pasteurization and must be the area where the wall and ceiling join controlled through other methods.) over the duct. Remember, the extreme This is especially true in the winter environmental conditions produced months when pests should be virtually during a normal mushroom crop, nonexistent. particularly during pasteurization, can be very stressful on a building. Cracks Exclusion, like monitoring, is often can develop that were not there during discarded when another “magic bullet” inspection prior to the crop. pesticide comes onto the market. The pesticide will give good control for a Building materials also are important. time, then resistance (See Section I.B) Because it is organic and porous, wood will begin to occur, reducing the can be a good hiding place for patho- pesticide’s effectiveness, or worse, genic organisms. Porous cinder blocks rendering the material useless. Exclusion and concrete also provide refuges for limits the number of pests exposed to a organisms, particularly in the floor, given pesticide, thereby reducing where it is nearly impossible to develop resistance. high temperatures. Consider inorganic,

21 smooth, dense construction materials Figure 9. Drain plugs must be sealed to keep out flies and especially rodents. whenever possible. Plastic and alumi- num are good choices, though cost often precludes their use. Inorganic insulation is a must. Sawdust, for instance, can become a breeding ground for pest organisms. Cost of materials must be weighed against potential benefits.

Don’t overlook the obvious entry points in any building, such as drain holes (Figure 9) or the webbing in blockwork. Unless the top of the wall is capped, there are thousands of passageways within the wall through which flies can pass.

In an existing facility, mortar and caulk are inexpensive alternatives to chemical pesticides or crop loss. When a growing room is empty, inspect for cracks and any other damage that may have Figure 10. Rooms can be sealed with urethane insulation. occurred during the crop. Buildings expand and contract from the changes in temperature during the crop. High humidity causes wood to swell. Where disimilar materials come together, such as wooden doorjambs against block walls, the different expansion rates of the materials cause cracks to develop between them. All of these areas must be inspected, sealed as needed (Figure 10), and marked off on a checklist. Turn off the lights inside the room and look for light penetration from outside. If a growing room has a spring roof, this area must be checked. Ceilings are especially susceptible to damage, particularly if the temperatures during pasteurization are allowed to get too high. High temperatures can damage insulation; sprayed-on polyurethane can buckle and crack. Nailed insulation sheets can buckle, pulling the nail heads through the insulation and leaving access holes through which pests can enter. Turn on the lights inside the room when inspecting a loft area and watch for light penetration. Pasteuriza-

22 tion at the end of a crop is also a good Figure 11. Filter material used to seal doors. time to check lofts, since steam will escape through openings in the ceiling. Mark these openings and have them repaired. This not only will exclude pest organisms, but will reduce energy costs as well.

Limiting and sealing access doorways is of particular importance. Only one or two doors in a plant or any mushroom building should be used as entrances. All other doors should be sealed. Doorways used for entrance and exit must be sealed around the edges, and there should be a threshold at the bottom to seal the door when closed. Seal these doors with weather-stripping or strips of filter material (Figure 11). Spray the sealed edges with oil or adhesive as an additional barrier against pest entry. A step mat with a sanitizer should be placed at the entrance to sanitize shoes. Clean the mat regularly or it could become a source of infesta- tion. It is better to not have any mat than to use a dirty one. Entrance doors into the growing rooms should be treated the same way as the entrance to the hallway or the plant itself. If there is more than one door into the growing room, one of them can serve as the entrance and the others can be sealed completely. If doors must be kept open for ventilation during Phase II, they should be covered with fly netting or filter material. fibers. The fly will move the fibers back Obviously, filter media must be imper- and forth and work its way through vious to fly penetration. What may look material that looks impenetrable. Only impervious to us may not be to a fly. by testing the filter material or fly Flies can get through much smaller netting can a grower be confident flies holes than their body size suggests. cannot get through it. Filter media offer an additional prob- lem. The structure of most filter media makes it ideal for collecting dust particles, but also for active pests, such as flies, to work their way through it. When a fly comes in contact with filter material, it sees a mass of hair-like

23 There are other considerations for need more filter surface area to allow Choosing Filter and Fly choosing filter material instead of the fan or blower to deliver sufficient Netting netting for a particular application. air. Typically, the pressure drop for the With netting, excluding flies is enough, filter should not exceed 1.0 inch of Testing can be accomplished in a variety but filters are expected to remove spores water. Filters must be tested at the of ways. First, inspect the material. and dust particles. Spores of concern in mushroom house to ensure they do not Holes large enough to permit the mushroom cultivation are from two to restrict the air too much. Also, the filter passage of flies may be obvious. Netting ten microns in diameter. (A micron is must be able to withstand the rigors of or filter media may be manufactured one millionth of a meter, while a typical mushroom house installation. Paper inconsistently, allowing some of the spore is about one ten-thousandth of an filters are very efficient but cannot be openings to be larger than others, or a inch.) used in the moist atmosphere of a mushroom house. Therefore, filters filter may have thin areas or “windows” When deciding which filter to use, you made from glass fiber or other synthetic insects can pass through. The material should know what quantity of dust and materials are preferred. Some manufac- may not be strong enough: i.e., people spores a filter can trap, in addition to turers also coat filters with a viscous working near netted openings may knowing that it can exclude flies. material known as a tackifier to aid in damage it too easily. Testing is not an easy task on commer- trapping particles. Second, test the filter or netting for fly cial farms. Instead, ask the supplier to penetration. One method to accomplish provide test data concerning particle size Once a suitable material is found and this is to wrap the netting or filter removal using a standard ASRAE attached to a door, filter frame, or other media in question around a wire frame (American Society of Heating, Refriger- opening, the edges must be sealed. and place a known number of flies ating, and Air-conditioning Engineers) Gapped, loose, or bunched edges of inside. Seal the material with a twist tie test. These are standard tests of which filters or netting are excellent or string and place it outside (where the the most common is the “weight entranceways for flies, and the filter is flies can’t have access to new growing arrestance test,” that uses standard test rendered useless if a good seal is not rooms) or inside an old room that has dust and will show the percent effi- made there. Flies are tenacious in their flies, and determine if they escape. ciency of the filter media at removing attempts to enter a mushroom house, Conversely, you could place something particles by weight. Typical fibrous and they have nothing to do all day but the flies want inside the material and filters have efficiencies of 60 to 80 look for ways to get inside. They can determine if they can penetrate it. Try percent, with some reaching 90 percent smell compost and will mill about the placing fresh spawned compost or a fly of the test dust trapped. HEPA filters outside until they find a way inside. light equipped with flypaper inside a are the most effective at removing small Insects will follow the path of least box to capture invaders. Use an open particles and commonly have efficien- resistance; a fly walking along a wall will topped box with sealed seams and place cies greater than 99.97 percent. This is not climb around or over the seam, but freshly spawned compost in the bottom the percent of the total weight of the will go under it if there is an opening of the box. Place flypaper on the top of dust that is trapped and does not relate between the material and the wall. The the compost, sticky side up. Or, attach a to a specific particle size. A filter with a simplest method to seal the edges is to fly light with flypaper to the bottom of rating above 60 percent efficiency fold over the material and staple the the box. Cover the open side of the box usually will remove all particles of less edge directly to the doorjamb. Replace- with the material and seal it with duct than five microns. able boards attached to the doorjamb as a stapling surface will extend the life of tape. Make sure there are no openings The higher the efficiency of the mate- the jambs. Narrow slots into which the in the box or at the seals where flies rial, the better the dust exclusion, but material is pushed or even Velcro can could get through. If a fly light is used, high-efficiency filters will cause more air create effective seals. Regardless of the an opening must be made for the power restriction than low-efficiency models. method selected, a good seal is para- cord. Be certain this is sealed. Put the In general, higher-efficiency filters will box in an old, fly-infested room. If the mount. Workers performing the test material is impervious to fly entry, installation must be trained to make no flies should be found on the paper. sure the material is sealed and not simply installed.

24 Additionally, an adhesive like Tangle when spawn is transported to a room, it time. No tools should be required Trap improves the edge seal. Flies snared first should be unloaded into the during installation. Simple, hand- by the adhesive not only are incapable breezeway via the entrance door while tightened turnbuckles can draw the of crawling under a filter but also are all room doors are closed. Once all the foam tight against the wall and jamb. prevented from finding other cracks. boxes are inside the breezeway, close the Pay close attention to mated surfaces This is more important than it may outside door and open one room door after installation. Improper installation seem, since you probably never will to put the spawn into the room itself. provides entry points for flies. Lastly, succeed in sealing all of the cracks in a While the door to the outside is open, spray the edges with fly trapping building. Spray adhesive on netting and direct fans at the doorway to help material. filter seams, doorframes, fan openings, prevent dust from drifting inside and to Though not as susceptible to disease and filter frames. break up the flight paths of any flies organisms as cooldown and spawning, that may try to pass through. There are times when an entranceway the casing operation and casing prepara- must be opened for a very good reason Portable air conditioners required at this tion can have pest problems. Phorid early in the crop cycle, for example time usually are installed in an outside flies are attracted to actively growing during the three days before and after door presenting additional exclusion mycelia, and Verticillium spores can spawning. Unfortunately, this is the challenges. Until installation and sealing infest the casing. Take the same precau- most critical time for fly control in the are complete, flies, spores, and dust have tions during these operations as you use crop cycle. Fresh Phase II compost is a direct and unimpeded path into the during spawning. very attractive to the female sciarid fly, growing room. Installation, therefore, Exclusion also involves controlling the and the compost is very susceptible to must be quick. The unit should be on movement of people and equipment. green mold colonization at this time as wheels, and methods should be devised Anyone who has been in older rooms— well. (This will be discussed thoroughly to get it installed and sealed quickly. harvesters, maintenance people, in later sections.) But this is also the Attach a sheet of plywood with a border supervisors—must not be allowed to time when spawn and supplements, of foam rubber to the front of the enter new rooms they could infest by spawning equipment, and other items portable unit so it can be wheeled bringing in contaminated casing or must be brought into or taken from the against the wall and sealed at the same rooms. Often, a portable air conditioner must be installed in one of the doors to Figure 12. Movement of employees between “clean” and “dirty” areas must be help cool the room. When performing controlled. these tasks, limit the time the door is open and take precautions to prevent infestation or contamination.

When employees bring equipment or materials into the growing rooms, they must keep doors closed when not actually entering or exiting the room. Train them and remind them con- stantly. Teach your employees the importance of keeping doors closed. On the other hand, an automatic door closer, even something as crude as a spring, rubber strap, or counterbalance, will help significantly to prevent fly entry if open doors are a problem on your farm. Also, train employees to recognize and eliminate straight flyways. If a breezeway door is open, all room doors should be closed. For example,

25 compost, spores, flies, or mites (Figure 12). Harvesters should have lunch and References break areas separate from employees who work in clean areas. Always assume Lomax, K. M. 1998. Air filter selection. that areas are contaminated if fre- Mushroom News 46:14–16. quented by harvesters or people working in other dirty operations such as Phase I compost filling. These areas must be sanitized periodically, and of course are always off-limits to people who work in clean areas.

Equipment used in older rooms—hoses, spraying equipment, harvesting equip- ment—should not be used in clean rooms. Make separate clean and dirty room equipment available. If a piece of equipment must be used in both clean and dirty rooms, sanitize it thoroughly before using it in a clean area. For example, always use spraying equipment for pesticide applications in clean rooms first and then in progressively older rooms. Of course, the equipment must be sanitized before use in clean rooms the next day.

Exclusion continues to be important toward the end of the crop. At this stage, instead of trying to keep pests out, they must be kept inside the growing rooms. Exclusion now is more aptly called containment. Flies are actively seeking ways out of the growing rooms, looking for fresh compost or growing mycelium, and are most likely carrying pathogenic organisms. Though not as critical as the employees in the spawning operation, harvesters also must be trained to keep doors closed. Filters must be kept intact. Filter exhaust air as well, to prevent expulsion of spores and flies into the outside air.

26 A. Specific Control Techniques

Mushrooms are saprophytes, part of a and mushroom mycelium is aseptically group of decaying organisms that are transferred into them. Composting is 2. Cultural Control nature’s “janitors.” Together with other required to make the material pliable so decaying organisms (various bacteria, it will hold sufficient water to sustain Phillip S. Coles molds, etc.), mushrooms (fungi) the mushrooms through the crop and to eliminate dead material in nature. If not create enough density to allow trays or William Barber for the action of these “janitors,” the beds to be filled with the desired dry world would be buried in dead plant weight at a reasonable depth. However, and animal material. the most important reason for composting is to make the materials In nature, it might not matter which selective for mushroom mycelium organisms consume dead leaves or a (Figure 13). fallen tree, but in trying to grow a specific fungi, the environment must be If mushroom mycelium is added to manipulated. This is possible with uncomposted materials—materials that specific cultural control techniques. are not selective for it—competitor Proper use of cultural controls can organisms will quickly take over. They manipulate growing environments to are able to grow much more quickly favor the cultivated mushrooms and to than mushroom mycelium and will discourage competitor organisms or exclude the mushrooms through rapid pathogens. Mushroom mycelium can growth, heat production, or production overcome a weed mold, for example, if of antibiotics (chemicals that prevent the weed mold is put at a disadvantage. the growth of other microorganisms No other means of control are needed if such as fungi and bacteria). Most environmental manipulation is success- microorganisms produce antibiotics as a ful or the competing organisms are form of chemical warfare to control weakened to the point that they become their territories. (Penicillin is a good susceptible to other controls such as example of an antibiotic produced by a pesticides or biological agents. fungus, in this instance by Penicillium mold.) Composting changes the raw Many common IPM practices are not materials, making them more attractive normally thought of as cultural controls. to the mushroom mycelium and Phase I and II composting, for instance, allowing the mushroom to outcompete are good examples of cultural controls. the competitors. Composting, therefore, Mushroom mycelium will grow readily is a form of pest control, and as such is on many of the materials used to make part of any good IPM program. compost if those materials are auto- claved (sterilized in a sealed container)

27 Figure 13. Making selective compost is one of the most important components of cultural controls and IPM.

In nature, a succession of organisms molecules. The more complex carbohy- These organisms will ensile the com- work together to decompose organic drates are saved for a later time when post. This is desirable in a silo where matter, and a similar process takes place the mushroom mycelium is introduced, materials are placed with the intention when compost is made and mushrooms because unlike many of its competitors, of excluding oxygen and growing are grown. Mushrooms are simply one mushroom mycelium is capable of organisms that will ensile the material of the organisms in the succession, producing enzymes that can break down so it will “keep” and can be fed to cattle though it is imperative that mushrooms these larger molecules. The presence of at a later date. However, this is com- are introduced at the right time in the these large molecules, after a properly pletely undesirable when producing sequence. When raw materials come to managed Phase I, is one of the charac- mushroom compost. Anaerobic organ- the compost wharf, they should be dry teristics that makes compost selective isms in mushroom compost make the to prevent microbial action and decay. for mushroom mycelium. Another compost selective for other types of Once they are wetted, the composting characteristic is the conversion of organisms by “keeping” the nutrients in process begins. The first organisms to ammonia, by the action of compost the wrong form and by producing grow are the opportunists, fast-growing microflora, to microbial protein. This anaerobic compounds that are difficult microbes that release a lot of energy, stage is Phase II composting. to break down during the composting

CO2, and water. This causes the cycle. Regardless of when they are compost to become hot and explains It is not enough simply to allow produced in the composting process, why it requires abundant oxygen. If composting to proceed uncontrolled. If anaerobic compounds are toxic to composting is done correctly, microbes composting materials are too dense or mushroom mycelium if they remain will produce ammonia and concentrate too wet, air will be excluded and after Phase II. simple carbohydrates into larger anaerobic organisms will begin to grow.

28 Figure 14A. Relation of temperature to growth rates of a typical psychrophile, a typical mesophile, a typical thermophile, and two different hyperthermophiles. The temperature optima of the example organisms are shown on the graph.

Thermophile Hyperthermophile Psychrophile Example: Example: Example: Bacilus Thermococus celer Pyrolobus fumaril

Growth Rate Growth stearothermophilus Mesophile Example: 60o 106o Escherichia coil 88o

39o 600

Psychrophile Example: Polaromonas vacuolata

4o

0102030405060708090100 110 Temperature (oC)

Figure 14B. The effect of temperature on Temperature is a good indication of Length of composting in either extreme growth rate. what is occurring inside the compost can have results similar to under- and pile (Figures 14A and 14B). High over-supplementation. If Phase I is too Optimum temperatures indicate that aerobic short, excess carbohydrates will remain. composting is taking place. Low If it is too long, energy will be depleted

Growth Rate Growth temperatures, on the other hand, can be until not enough remains in the an indication of anaerobic composting. compost for conversions required in Phase II. Compost formulation is an important part of IPM. If the formulation is incorrect, excess nutrients will be left in Minimum Maximum the compost. If nitrogen supplementa- Temperature tion is too high, for instance, excess ammonia will be produced. Ammonia above .05 percent is toxic to mushroom mycelium and promotes the growth of undesirable fungi like Coprinus. (Section II.C.3.) Conversely, supplement compost with too little nitrogen and simple carbohydrates will remain (residual) in the compost after Phase II. Excess carbohydrates promote the growth of fast-growing competitor organisms like Aspergillus, which will overtake mushroom mycelium.

29 Phase II Pasteurization Temperature and Humidity Control In Phase II, an entirely different set of Pasteurization is another critical pest organisms grow. These organisms control step in Phase II. Compost can During spawn run, optimal temperature consume ammonia and convert it to contain many types of pathogenic is again very important. If the compost protein. Ammonia contains a nitrogen organisms. Nematodes are the most temperature is too low, mushroom molecule that is essential to protein common, but other types of molds and mycelium, obviously, will grow slowly. formation, and the Phase II organisms their spores also are present. Proper Although growth of pathogenic organ- are capable of obtaining this molecule pasteurization ensures their destruction. isms also will be slowed, their growth from ammonia. Later, these organisms Compost pasteurization serves the same will not be retarded as much as that of will become the protein source for purpose as the pasteurization of milk. mushroom mycelium. High tempera- mushroom mycelium. They also use the Temperatures are raised sufficiently and tures are a greater problem. They not remaining simple carbohydrates left for an adequate time to ensure the only will weaken or kill mushroom over from Phase I as fuel. The impor- destruction of pathogens, but are low mycelium, depending on the tempera- tance of the Phase I formulation should enough to allow the survival of benefi- ture ultimately reached, but also will be apparent. cial microflora. By pasteurizing rather promote the growth of heat-producing than sterilizing, which is done at competitors. These make temperature Just as Phase I can fail due to manage- temperatures that will destroy all control more difficult. To make matters ment practices, incorrect temperature organisms, surviving beneficial microf- worse, dead mushroom mycelium management in Phase II can spell lora help to exclude pathogens that later becomes a source of simple sugars, disaster for pest control. If the tempera- may be introduced to the growing providing food for the competitor tures are too low or too high, ammonia- room. The microflora exclude patho- organisms. converting microbes will be unable to genic organisms by “tying up” sites, or It is not adequate to rely on a good perform effectively. If temperatures in prohibiting pathogens from obtaining “average” temperature. The average of the compost are too high, for instance, substances they require, such as food. 110°F (43°C) and 40°F (4°C) is 75°F Phase I conditions will recommence and They also are capable of producing (24°C), but neither temperature is ammonia production will continue. antibiotics, which can destroy patho- conducive to optimal spawn growth. Furthermore, the organisms that thrive genic organisms. The microflora Hot areas must be located and con- at high temperatures and produce population remaining after pasteuriza- trolled before they spread and cause ammonia will use some of the simple tion is important, therefore, to the severe localized damage similar to the carbohydrates the Phase II ammonia- successful completion of Phase II damage occurring in an entire room converting organisms will need. There composting, but also serves as direct that has overheated. will not be enough simple carbohydrates competition for invading pathogens. (energy) for these organisms to convert After casing, while temperature remains the ammonia. They literally will run out important for reasons similar to spawn of food, and the unconverted ammonia run, there are additional considerations will cause problems for the mushrooms. as the crop progresses. If temperatures If temperatures are maintained at levels are raised to promote early maturation that are too low, ammonia-converting of mushrooms, other organisms such as microbes will not survive, since they Verticillium can increase their popula- require specific temperature ranges to tions very rapidly. Although the elevated flourish. temperatures may cause the mushrooms to mature more rapidly, Verticillium will spread even faster.

30 Relative humidity control, as most growers realize, is important for overall Shortening Crop Cycles Sanitation mushroom quality, but it is also an important part of IPM. A film of water Any technique that shortens the length Sanitation is essential for controlling on wet mushrooms provides an ideal of the crop cycle aids pest control by mushroom diseases and arthropod pests, habitat for Psuedomonas tolassi, the reducing the amount of time pathogenic because it will slow the spread of causal agent of mushroom blotch. organisms have to reproduce. The pathogenic organisms as well as lower Maintaining dry mushroom surfaces is strategy is to complete the harvest and their overall populations in the mush- the most effective method for prevent- pasteurize the room before pest popula- room-growing environment. The place ing blotch, and relative humidity tions can damage the crop. The benefits to start is outside the growing rooms. control is one tool for accomplishing are twofold: first, when pest organisms Roads and the immediate vicinity of this. (See Bacterial Diseases, Chapter enter a growing room, they do not have mushroom houses should be paved with II.C.4.) sufficient time to reach economically concrete or macadam, since dust is an injurious levels within that crop. excellent carrier for the sticky spores of Second, it reduces the amount of Verticillium or Trichoderma. Areas innoculum on the farm for new crops in around growing rooms, tunnels, and other rooms. This applies to arthropod other sensitive locations should be kept pests as well as fungal pathogens. free of dirt. In dry weather, water to keep dust to a minimum. These areas, There are many ways to reduce the time also, should be kept free of clutter. needed for the cropping cycle. Most Debris provides hiding places for flies, important, run the growing rooms sheltering them from inclement properly from the start. Low tempera- weather. Mow grass to reduce areas tures or mechanical problems in where flies can hide from sun, frost, or spawning or casing can delay the onset rain. of picking and expose the room to excessive increases in pest populations. The walls and floors of rooms must be Phase II rooms must be brought into washed and sprayed with sanitizers to conditioning range without undo delay. ensure all pathogens are destroyed. Cooldown-to-spawning times should be Steam pasteurization within a room is kept to a minimum, and proper not sufficient to ensure these surfaces spawning rates must be used to ensure are free of pathogens, since the walls complete colonization in a minimal and floors act as heat sinks. Heat is amount of time. During cropping, conducted through the floor into the remaining mushrooms from each break ground, which has an almost infinite should be stripped to help the next capacity to absorb heat, maintaining the break come in more quickly. floor cooler than the room air in contact with it and ensuring such surfaces will Growing techniques that shorten crop never attain pasteurization tempera- cycles also should be considered, such as tures. For the same reason, the basement adding CAC-ing (Compost At Casing) floor of a house always will be cold to the casing layer and reducing the unless it is insulated. number of breaks. Through-spawning and supplementation are examples of methods used in the past to shorten crop cycles.

31 The importance of washing before room is heating up. If fly populations sanitizing cannot be overemphasized, are very high, the room should be because any dirt left on a surface quickly sprayed with quick knockdown ties up a sanitizer. This renders it insecticides to prevent escape once the ineffective and essentially protects any steam is turned on. After steam-off has spores or other potential pathogens started, monitor both compost and air from being destroyed. temperatures with probes. Raise the air temperature with live steam to 160°F Hallways can harbor carry-overs from (71°C) and maintain it there until the previous crops. All hallway surfaces compost reaches the same temperature. must be washed and sprayed. Any areas Begin counting time when the that cannot be sprayed, such as electric compost reaches 160°F (71°C). The panels, must be wiped down with a compost temperature should be 160°F cleaner and disinfectant. (71°C) for at least 5 hours to ensure an Once growing rooms are clean, they adequate kill of all pathogens. If must be maintained that way. This pathogenic organisms are found to be would be easy if they could be sealed, surviving steam-off, wet the casing but people and equipment must enter surface before injecting steam to help rooms to perform mechanical opera- with heat transfer through the compost tions and monitor the crops. The and casing. Also, more time can be movement of equipment and people on added to the steam-off. a farm must be controlled. Equipment, for example, should be separated and color-coded according to department or use to ensure that dirty equipment such as squeegees from filling operations can’t be used in clean areas.

Within the room, good housekeeping minimizes the multiplication of pest organisms. Keep growing surfaces free of organic matter such as dead mush- rooms, which can serve as food sources for pest organisms. Mushrooms should be picked tight to reduce the chance of spreading spores containing virus particles.

Steam-off is an important part of maintaining low pest populations. During cropping, pest organism populations will increase inside the house and are potential sources of contamination for new growing rooms. Steam-off, or post-crop pasteurization, eliminates these contamination sources. Prior to steaming, growing rooms should be closed, and openings such as those for fans should be closed to prevent the escape of pathogens as the

32 A. Specific Control Techniques

part of existing pest control practices. Introduction The IPM program would be alert to this 3. Biological possibility. Application of the biocontrol Control Biological control provides the mush- agent would be withheld until chemical room grower with natural tools to residues have dissipated, or a control Danny Lee Rinker control mushroom pests. Natural anti- agent may reproduce more slowly than pest capabilities of nematodes, wasps, or the pests and never “catch up” once the bacteria are exploited. Biological control pest population is high. An IPM also capitalizes on the properties of program then may include other means, chemical substances released by the pest perhaps chemical controls, to lower the or by food on which it is feeding. pest numbers. The biological system can be left to do what it does best— Biological control methods offer many maintain low pest populations. advantages over chemical control: the agents have a specific host range, there An IPM program can help the farmer are no toxic residues, and concern for manage other limitations of the biologi- worker exposure is reduced. Biological cal control method—longer time to control methods can target a pest and peak effectiveness, incomplete elimina- reduce its numbers to an acceptable tion of the pest, cost, and inability to farm operational level. In addition, the overcome the overwhelming pest control agent may be self-perpetuating, pressures resulting from poor house- reducing the need for frequent reappli- keeping—by calling for other control cations. Development of resistance is measures when they in turn are most rare. effective. And, because biological agents may have detrimental effects on the Biocontrol requires the support of an mushroom crop if applied improperly IPM program to create the conditions or when their use is not warranted, an under which biological agents can be IPM program must be in place to most effective. For example, the agent ensure that the biological agent serves may act only against an immature stage the grower’s needs while avoiding of the pest and have little impact on the reductions in crop yields or quality. adult, necessitating that the IPM When supported by an IPM program, program call for its use when the biological control methods can expand immature forms are predominant in the the mushroom farmer’s arsenal of pest pest population. Or the biocontrol control weapons. agent may be more susceptible than the pest to pesticides and may be killed or weakened when pesticides are used as

33 Biological control programs in the Parasitic wasps must be integrated mushroom industry are currently being within a pest management program. Sciarid, Phorid, and Cecid used for nuisance flies on compost Reducing conditions favorable to Management wharves, sciarid flies, and blotch disease. breeding helps to limit fly populations. Additional potential agents for biologi- Flies will reproduce in moist organic Mushroom fly pests are a consistent cal pest management in the mushroom matter; therefore, promote good problem for growers. The three fly industry are cited. drainage, remove seepage, and minimize groups most commonly encountered are standing water to lower the number of the sciarid fly (Lycoriella mali), the nuisance flies. Good sanitation on the phorid fly (Megaselia halterata), and the wharf, rotation of raw materials, and Nuisance Flies on Compost cecid fly (Mycophila speyeri, Heteropeza removal of spent substrates from the Wharves pygmaea). The sciarid larvae attack farm also will expedite fly management. compost, spawn, mycelia, pins, and Routine fly monitoring is essential to The house fly (Musca domestica) and the mushroom stems and caps. The larvae evaluate the necessity and effectiveness stable fly (Stomoxys calcitrans) are of phorid flies feed on mycelia, causing of a management program. Release rates common to compost wharves. An depressed crop yields. Cecid larvae feed of parasites are dependent on fly effective biocontrol method augments on the mushroom stems or gills, numbers, environmental and climatic the number of naturally occurring reducing marketable yield. Sciarid and conditions, migration from off-site Pteromalid wasps. These tiny wasps are phorid adults carry disease organisms locations, and chemical controls. parasites that attack the immature pupal into the crop. Mushroom flies are discussed in greater detail in Chapter stage in the fly’s life cycle. The wasps are Wasp release early in the season is a II.C.1 of this manual. nocturnal and do not sting. Commonly good strategy, since the fly pests have used species are the Spalangia endius, certain survival advantages over the Muscidifurax raptor, M. zaraptor, and M. wasps—greater reproductive capacity, Nematodes as Control Agents Against Mushroom Flies raptorellus. ability to fly greater distances, and greater resistance to pesticides. If the The Pteromalid wasp has a life cycle Mushroom flies are good targets for number of adult flies is too high, bait similar to other insects: egg, larva, pupa, biocontrol with beneficial nematodes. trapping can initially reduce it. Once and adult. Most of this wasp’s life cycle More information on nematodes, the adult fly number is lowered, the occurs within a host that provides especially those that negatively affect the wasps can be used to keep the pests nutrition and protection for all stages mushroom crops, can be found in under control. other than the free-living adult wasp. Chapter II.C.5 of this manual. Benefi- House flies and stable flies are among cial nematodes, those that can play a their potential hosts. The adult wasp role in biological control, are covered lays her eggs into the nuisance fly’s here. pupa. The immature parasites consume Howardula husseyi as a Control the host’s tissues from the inside, and Agent Against Phorids adult wasps “host feed” on fluids from Howardula husseyi is an endoparasitic the outside, preventing the fly from nematode that occurs naturally in the developing into a healthy adult. The phorid population. This nematode lives wasp’s life cycle requires two to four both in the compost and in the fly. It weeks. Under optimal conditions, the has a six- or seven-stage life cycle: egg, parasites can reduce the nuisance fly four or five immature larval stages, and population in 4 to 6 weeks. Complete adult. Some of these immature-stage elimination of flies usually is not larvae are free-living, while others are possible, especially where there is parasitic. Both adult male and female migration onto the farm from off-site phorids are commonly infected with locations. nematodes.

34 When the female phorid attempts to lay the new bacterial cells and host tissues Mites as Control Agents against eggs on spawned mushroom compost, and then develop into adults. The adult Mushroom Flies she also deposits second-stage nematode nematodes reproduce in the host. Young A predator consumes its prey, either larvae. Female and male nematode nematodes, finding the food supply partially or entirely. One such predator larvae develop and mate while in the depleted, will exit the cadaver. in the mushroom crop is the mite compost. The fertilized fourth-stage Infective-stage nematodes can be Hypoaspis miles. This mite will prey females (“infectives”) enter the phorid upon larvae of cecids, phorids, and larvae or young pupae and develop into applied to the casing material at casing or later during the crop. The nematodes sciarids. These mites are commercially adults while in the phorid body cavity. available for use in the greenhouse While inside, they also deplete and do not feed in the compost or casing. They can be responsible for high levels industry, but none are being used at this disorganize the fly’s food reserves and time in the commercial mushroom lay eggs. After the eggs hatch, the young of mortality among L. mali larvae. Lab trials have shown S. feltiae to cause industry. The mite is less than 1 mm in nematodes work their way through the size and light brown in color. The life phorid ovaries into the oviducts. When mortality levels up to 100 percent. On- farm trials have attributed lower, but cycle is complete in about two weeks. In the female phorid attempts to oviposit, small-scale experimental trials, sciarids she discharges the nematodes. significant, reductions in fly emergence (e.g., 66 percent fly emergence) to the were controlled at 96 percent using 750 2 While in the phorid, the growing and pathogenic effects of S. feltiae when mites per m . However, field trials in developing nematodes reduce the applied at rates of 81 million nematodes Ontario were not as dramatic, with less phorid egg production by 50 to 100 per 100 m2. In order to achieve higher than 30 percent control of sciarids. The percent. Under controlled lab condi- mortality, current supplier recommen- mites do not suppress mushroom yield, tions with parasitism increasing uncon- dations are 300 million per 100 m2. nor are they found on mushrooms. trolled, phorid populations can be Mites have several advantages. They are virtually eliminated within five fly Microorganisms as Biological mobile and can easily search for prey; generations. Commercialization of this Control Agents of Mushroom mushroom growing conditions are nematode species has not been success- Flies suitable for their reproduction; and they fully achieved. can live for several weeks without food. Bacillus thuringiensis subspecies Despite the low control rate thus far, Steinernema feltiae as a Control israelensis (Bti) is a bacterium that is predatory mites do have potential for Agent Against Sciarids used widely in biocontrol. The bacte- successful integration into biocontrol of A beneficial entomopathogenic nema- rium produces both a protein crystal mushroom pests. tode, Steinernema feltiae, has been and a spore. Once eaten by the larva, impressed into service as a biocontrol the crystal degrades in the alkaline gut Fungi agent against sciarids. This nematode of the insect. The insect’s gut subse- species carries bacteria that are deadly to quently becomes paralyzed, and larval Some fungi are capable of invading the the sciarid fly. Bacteria live within the death occurs within 48 hours. bodies of flies. The pathogen spore or gut of the nematode and are released mycelium penetrates, develops, and kills Field trials have demonstrated control of once inside the host. The nematode life the host. After death of the host, spores phorids and sciarids when Bti was cycle includes the egg, four juvenile are produced on the cadaver’s surface. applied either to compost or casing. stages, and the adult. The third juvenile These spores then will infect others. The Small-scale research trials with one stage generally enters the third or fourth development of Pandora gloeospora has formulation have demonstrated that a larval stage of its host through natural shown promise for control of sciarids. compost application could provide 85 body openings like the mouth, anus, or percent sciarid control. An application spiracles, or it may go directly through to casing at a lower formulation rate the body wall. Once inside the host, the manifested a 70 percent control level of nematode makes its way into the body sciarid larvae. Excessive mycelial growth cavity of the insect larva and releases the on the casing or reductions in yields bacteria. These bacteria rapidly kill the may occur from a casing application. host within 48 hours by blood poison- Bti appears to be more effective against ing. The immature nematodes feed on younger rather than older sciarid larvae.

35 Repellants and Anti-Feedants

Biologically Derived These chemicals act as a “self-defense” Conclusion Chemicals Used in mechanism for the food source. They Biological Control of either repel the pest from the food Biological control of mushroom pests is Insects source before it feeds (repellant) or a reality. Parasitic nematodes and wasps afterwards (anti-feedant). Calcium are commercially available and are The term “biological control” has come oxalate, a byproduct of mushroom becoming integrated into pest manage- to include the use of chemical sub- mycelial metabolisms, has been found ment programs, while other organisms stances with control potential. In some to have repellant activity toward the including fungi, bacteria, and mites are cases, insects themselves may be the larvae of sciarids. By itself, calcium being developed. The prospects are source of the chemicals that will attract oxalate is not an effective control favorable for the development of others. Or, substances can be produced method, but as part of a wider program, effective biological control agents in the by the food source that may either it may prove to be useful. next several years. attract or repel insects.

Pheromones Disease Management Pheromones are volatile chemicals that help insects find each other or cause Most biocontrol efforts against some other biologically important mushroom diseases have focused on response. The compounds are species bacterial blotch. Bacterial blotch specific and are detected by the insect in disease, caused by Pseudomonas tolaasii minute concentrations. In a biological or P. gingeri, has been managed control program, these chemicals are commercially by another bacterium (P. used to attract large numbers of the fluorescens biovar V). The biocontrol pests (mass trapping) to stop an agent acts as a preventative, becoming infestation or, conversely, to confuse the established before the development of pests so the two sexes cannot find each a blotch population. It competitively other to mate. Sex pheromones have excludes the colonization and develop- been demonstrated for phorids and ment of the blotch population. sciarids. However, commercial trials Bacteriaphages (viruses that infect using synthetic compounds have not specific bacteria, usually killing them) also have been used successfully been successful. against blotch. Combining both organisms could be highly effective. Kairomones

Kairomones are volatile chemicals produced by a pest’s food source that alert the pest to its presence. They could be used as a chemical message to lure pests into traps. The attractiveness of compost to sciarids during Phase II cool-down or of actively growing mycelia to phorids are observed events. However, researchers have not been able to duplicate the phenomenon observed in the field.

36 A. Specific Control Techniques

Integrated Pest Management is not thresholds and temperatures, and never synonymous with organic or pesticide- on a rigid schedule. Also, pesticides are 4. Chemical Control free production, as many people believe. most efficient if used when they can Judicious use of chemical pesticides is lower a high pest population rapidly Phillip S. Coles an integral part of an IPM program. In and significantly, providing the grower IPM, pesticides are not applied on a the opportunity to get the pest under rigid schedule as they are in a chemi- control and possibly saving a crop cally dependent pest control program. obviously in peril. Other IPM strategies They are one facet of a broad (inte- then can maintain that level of control. grated) approach to pest management, though one that frequently can be There are two pesticide application minimized or avoided altogether. techniques on a mushroom farm. One is preventative, and is predicated on Many pesticides appear to provide monitoring and temperatures, while superb pest control independent of monitoring exclusively triggers the other control measures. After an other. Preventative applications serve application of a contact material, for the same role as physical exclusion. instance, many dead insects may litter Instead of making it physically impos- the outside of a plant, tempting sible for fly entry, however, a chemical complete reliance on such products. barrier is applied in an attempt to kill After a simple (though not inexpensive) the fly before it gains access to the application, the grower feels good. The growing room. This is not as effective as application complete, there is now more physical exclusion, but it is a backup to time to devote to the long list of other it if some entry points have been duties that confronts a grower each day overlooked. Use a contact poison for on a mushroom farm. Regularly this application. There are other types of scheduled pesticide applications, pesticides, but more on them later. therefore, become appealing. Preventative applications do not replace But using chemical pesticides in this diligently sealing the growing room. On fashion is destined to develop pest the contrary, the two must work resistance to them. Pest organisms together. (See Chapter II.A.1, Exclu- readily become resistant to overused sion.) If a contact spray were used chemicals. (See Chapter II.B, Resistance without physical exclusion, only the management.) Pesticides in an IPM most resistant flies would be entering program, however, are applied as a last the rooms to reproduce. In effect, you resort and are used in accordance with would be screening for “super flies.” monitoring, established economic

37 Only use spray when weather is condu- A common use for preventative sprays is supplies. Never spray when there is a cive for fly movement and when applications to the outsides of buildings. chance of drift. significant fly populations exist on the Outside spraying, however, has serious farm. Every farm will be different, and disadvantages. It is difficult to get Chemical applications to enclosed areas each farm should develop its own complete coverage around and on top of outside of the actual growing area, such procedures dictating when spraying a building. It cannot be done during as hallways and lofts, are a more should take place. If the temperature is inclement weather. The pesticide is effective use of preventative sprays than below freezing outside and your exposed to the elements—rain can wash on the outer surfaces of buildings. Good growing rooms are physically separated, it off—and ultraviolet rays from the sun coverage is attained more easily; the flies cannot move from old to new break it down. There are also environ- material is protected from degradation rooms or from the wild population into mental concerns. The pesticide is and wash-off; non-target organism new rooms. Determine at what tem- outside where it can contact non-target exposure is limited; and the percentage peratures they will move on your farm, organisms, and care must be taken not of pest populations exposed to the and do not use preventative sprays when to contaminate streams or other water pesticide also is limited. This helps with the outside temperature is below the established figure. (See Chapter II.C.1, Figure 15. Fly light with many sciarid flies on it. Arthropod Pests, for flight tempera- tures.) You may want to decrease your threshold by a few degrees to add a safety margin.

Assess fly populations in two ways. First, population numbers should be available from monitoring inside the growing room. Have the numbers been high, or are they becoming high? Managers at each farm must decide just what is “high” when referencing monitoring data. Second, growers should have a good feel for fly popula- tions from time spent in the growing rooms. In early crop stages, usually it is not possible to detect flies without monitoring. If you can, you have a very serious problem! But, in the later stages of harvesting, high fly populations are detected easily. A grower must make spraying decisions with this informa- tion. An example of a spray-triggering scenario might be a daytime high temperature above 50° F (10° C), obvious fly populations in old harvest- ing rooms, and spawn run fly counts consistently above 10 flies per day. Obviously, the parameters would vary from farm to farm.

38 resistance management, since target monitor usually is placed above the It is important at this point to distin- organisms must penetrate the walls of highest bed so the light can be seen guish between different types of the growing building before coming in from a large portion of the room, as materials, for this will establish how contact with the pesticide. Logical well as near areas of the room where they are to be used. As stated earlier, targets for pesticide applications are penetration most likely occurs. Flies contact poisons make very good inside growing rooms, on beds or trays, should be counted daily and this preventative sprays. They are in place if and on any plastic covering the com- information used to make pesticide a fly tries to enter a growing room and post. Of course, pesticides used in decisions. Decisions can be made are effective against adult flies. A quick growing rooms must be labeled for according to daily or cumulative counts. knockdown material such as a pyre- mushroom use. Daily counts would trigger the use of a throid fog is very useful if flies suddenly knockdown material, an adulticide, appear on the monitor in cooldown or Despite exclusion and the use of while cumulative counts would dictate early spawn run. Larvicides and growth preventative pesticidal applications, the use of a larvicide in compost or regulators are good for mixing with the some flies still can gain access to a casting. compost and/or casing to prevent the growing room. To know whether flies flies from reaching adulthood and are entering a room—and the magni- Remember, a fly monitor does not catch producing another generation. tude of the invasion—you must all of the flies in a room. It traps only a monitor. The Pennsylvania Fly Monitor percentage of them. The monitor was provides the best way for commercial originally tried as a control method. It farms to monitor fly populations. This was hoped the flypaper would capture monitoring device is simply a black incoming flies, and that would be the light fastened to a board with a strip of end of them. After testing, only a sticky paper on either side of the light percentage of the flies were caught, and (Figure 15). The monitor should be these almost exclusively were females placed in a location proven to collect that already had laid their eggs. This the most flies of any area in the room. meant the monitor was useless as a The location will vary from farm to control technique; but by sampling the farm, necessitating some experimenting population, it gave a relative fly count at the outset. Keep in mind that flies for the room and therefore was valuable tend to be lazy and won’t travel far for making pest control decisions. unless it is necessary. Therefore, the

Type of Material Uses When to Use

Contact poison, adulticide Preventative, exclusional spray. Prior to air in growing rooms reaching 100° F (38° C), or before cooled compost is brought in a tray or tunnel system.

Quick knockdown, adulticide Good when large number of invaders When fly monitors indicate are present, or at the end of a crop when an influx of invading adults you want to prevent them from exiting a at the beginning of the crop, room and invading new rooms. or when the grower feels fly populations in an old room are high enough to threaten new crops. It also works well as a knockdown to prevent flies from escaping the room as steam is being injected.

Growth regulator or similar larvacide To prevent eggs laid by When cumulative fly counts invading adults from developing dictate their use. into adults, producing later generations.

39 An example of an economic threshold Establishing Economic for sciarid flies is two flies a day until Formulations Injury Levels the end of spawn run, then 10 per day through harvest. Obviously, higher There are several types of formulations Pest control decisions must be based on populations can be tolerated as the crop used for pesticides, each having its own monitoring. Even preventative sprays progresses (see Part I, Theory of advantages and disadvantages. Some have a monitor count component. Integrated Pest Management). This is pesticides are available in more than one Unfortunately, there are no concrete, also an example of a daily EIL. If more formulation, so their use can vary scientifically established economic than two flies per day appear on the fly depending on the situation. Most thresholds for mushroom farms. These monitor, the grower would be justified pesticides are available in only one numbers are somewhat arbitrary and in spraying a fogging adulticide to kill formulation, so their effectiveness must must be determined by the growers at the incoming invaders from that day. be weighed against the advantages of the each farm. If extensive scientific studies formulation. Cumulative counts determine the use of existed, there still would be dramatic larvicidal agents added to the compost differences from farm to farm, and and/or casing. High fly counts early in economic injury levels (EIL) would the crop would indicate future prob- have to be customized. Classes of Pesticides lems, since a significant number of the To develop individual EILs, the grower invading adults probably will be There are several classes of pesticides. must consider the level of potential successful in ovipositing in the compost. Some, like the organophosphates and damage. For example, sciarid flies cause A strategy is needed to prevent them carbamates, contain some of the original much more extensive crop loss than from producing subsequent generations. pesticides such as DDT. The more phorid flies, and can decrease quality by If a material is added to the casing layer, modern materials such as insect growth burrowing into the mushroom stems. there is more than adequate time for the regulators (IGR) are becoming more Therefore, higher numbers of phorids grower to make a control decision. For common. They also are safer than the than sciarids can be tolerated. There are example, if experience had shown that older materials and much more specific additional outside influences. If disease significant fly damage would result if in their range of effectiveness. The levels are low, a fairly high number of more than a cumulative total of 200 grower doesn’t have much choice in flies may be acceptable. But those same sciarid flies (a cumulative EIL) had what class of pesticide is used, since populations can be devastating if there entered a growing room prior to casing, only those registered can be used. Work are high levels of Verticillium and/or then a larvicide should be added to the with your sales representative to decide green mold on a farm. The sciarids are casing. On the other hand, if a material which ones are best for your applica- very important vectors of green mold, must be added at spawning, there is not tion. since they are most attracted to the as much time to make a pest control compost during cooldown, precisely the decision. In this instance, the material same time green mold infections are has to be applied before the spawning most likely to occur. When Verticillium machine mixes the spawn with the is high, only low populations of both compost, so the cumulative EIL would flies can be tolerated, keeping in mind be a specific number of flies on the that the high activity level of phorids monitor up to the day of spawning or makes them better at spreading the possibly until spawn broadcast. If a disease. All of these factors must be larvicide is added to the compost— taken into account when trying to either on the compost wharf or at fill— determine the economic threshold it is more similar to a preventative spray triggering a pesticide’s use. than a spray based on an EIL; therefore, preventative spray criteria would determine whether or not the larvicide was used at this stage.

40 Formulation Advantages Disadvantages

Emulsifiable Concentrate Easy on spray nozzles; can Cannot be mixed dry. (EC) A liquid formulation, be used with small amounts oil that makes an emulsion of water; easy to suspend in when mixed with water. water; very little residue left in bottom of tanks. Not dusty.

Wettable Powder—pesticide Can be mixed dry. Abrasive to nozzles. is mixed with clay carrier Difficult to keep suspended in used for suspending in water. water; much can end up wasted on bottom of tank. Dusty.

Flowable—a wettable Reduced dust as compared to Still abrasive to nozzles. powder that has been mixed a wettable powder. with a liquid to make handling easier.

Dust—a pesticide mixed Coverage can be seen and Dusty, dirty. Leaves a lot of visible with dust used as a carrier; evaluated. residue. very dilute compared to a wettable powder.

There are many simple ways to test Remember that flies are relatively fragile Testing pesticides. Fungicides are difficult to and do not live long, whether they are test because of the difficulties of exposed to pesticides or not. So you Finally, no pesticide, regardless of how working with the various pathogens. always should have a control group for safe or easy to use, is of any value if it Generally, insecticides are relatively easy purposes of comparison. If the unex- does not kill the target pest or pathogen. to test. The easiest are the quick- posed flies die, they may have been Pesticides must be tested, and they knockdown fogging materials. Make a mishandled. Try the test again. cage using fly netting that will prevent should be tested against the specific flies Once everything is in place to perform the flies from escaping, but that also will of a given farm. Just because tests show the test, flies must be collected. They are allow air movement. Place some flies good efficacy against sciarid flies for a very small and fragile, and collecting into the cage and hang it inside a room material does not necessarily mean it them is no easy task without the right that is scheduled for fogging. After the will be good against your farm’s sciarid equipment. The best way to collect flies room has been aired out, count the flies. Genetic variation occurs between is with an aspirator. Aspirators are number of dead and surviving flies. individuals and between different available commercially, some with populations. Generally, when a material There are several ways to evaluate battery-operated pumps. These are is new it will work well, but as it is used contact materials. It can be as simple as useful if you are collecting large (or misused) resistance develops, at placing wood blocks in an area that is amounts of flies on a regular basis, but different rates in different populations. being sprayed. Remove the blocks, place you also can fashion an inexpensive The only way to be confident in a them in a container, and add flies to the aspirator from some very inexpensive pesticide’s efficacy on your farm is container. If the flies die, the material lab materials that will suit the purpose through testing. works. Also, a lid to a container can be at almost any mushroom farm. All that Some testing is easy to do and can be fastened to a wall or ceiling, or simply is needed is a flask or bottle with a done at the farm level, while other tests placed on the floor. After it has been rubber stopper that has two holes. In are too difficult and require a profes- sprayed, fill a container with flies and each hole is a short piece of glass tubing sional. The expertise of the personnel on attach it to the lid to see how the flies with rubber tubing attached. One of the a given farm will dictate how much if do. This involves a little more risk, so pieces of glass tubing will have a piece any of the testing can and should be avoid taking flies into the growing of netting over the end inside the jar. To done there. room. Reserve this method for outside collect insects, suck on the end of the sprays. filtered rubber/glass tube while holding

41 the other rubber tube near the insect. It will be pulled inside of the jar for later Conclusion use. Be sure to place the netting over the end of one tube or you may end up Pesticides are an important part of any eating your samples! IPM program, but they also have drawbacks and should be used as a last resort after other types of controls have been put in place. They must be used in a responsible manner, not only from a safety and environmental standpoint, but also to ensure their continued effectiveness. A plan must be devised using monitoring and economic injury levels. The safest and most effective materials and formulations must be used, in the proper manner, and their effectiveness ensured through testing.

42 B. Pesticide Safety

Susan Whitney

The Worker Protection Standards Laws Regulating Pesticide (WPS) cover workers and pesticide Application handlers/applicators in mushroom production. (Workers are those employ- The Federal Insecticide, Fungicide, and ees who do any kind of work that would Rodenticide Act (FIFRA) requires bring then in contact with surfaces that certification and licensing of users of have been treated with pesticides in the restricted-use pesticides. Certification past thirty days.) All pesticides used in documents the fact that applicators/ mushroom production must have an handlers know how to use pesticides “Agricultural Use Directions” statement safely for themselves, the public, and the on the label. Read this statement to environment. There are two categories ensure that you are complying with the of applicators: private and commercial. law. For specific details on WPS, consult A private applicator is a person who uses the “EPA How-to-Comply Manual.” or supervises the use of pesticides for the The WPS requires employers to provide purpose of growing an agricultural the following for both workers and commodity such as mushrooms. The handlers/applicators: application can be done on property 1. Information at a central location owned or rented by the applicator or the that includes a WPS safety poster; applicator’s employer. A commercial the name, address, and telephone applicator is a person who uses or number of the nearest medical supervises the use of pesticides on a facility; and the name, date, time, “for-hire” basis. State pesticide inspec- restricted entry interval (REI), and tors with both the Pennsylvania Depart- application site of pesticides ment of Agriculture and the Delaware recently applied. Department of Agriculture routinely conduct on-site use observations to 2. Training for workers and handlers ensure that applicators are handling unless they are already certified pesticides correctly. Review the safety applicators. tips below in preparation for the pesticide inspector. 3. Transportation to an appropriate medical facility, as well as pesticide use information if a pesticide illness occurs.

43 1 4. Decontamination sites within /4 Figure 16. Applying pesticides using typical Personal Protective Equipment. mile of all workers and handlers. Supplies must include water for routine washing—one gallon per worker and three gallons per handler (in some cases, eye flush water must be immediately avail- able for handlers); plenty of soap and paper towels; and clean coveralls for handlers.

The WPS requires employees to provide the following for handlers/applicators:

1. Personal protective equipment (PPE) required by the pesticide label (Figure 16). Employers must confirm that all equipment is clean, is inspected for damage, and is working properly. PPE must be stored away from pesticides.

2. A pesticide-free area for changing clothes.

3. A decontamination site for washing after handling tasks and at mixing/ loading sites. Employers must monitor handlers who are using fumigants or any pesticide that has a skull and crossbones on the label.

4. Specific instructions on the pesti- cide label, including how to use application equipment. Employers must inspect and maintain applica- tion equipment. Employers must provide access to labels.

44 The WPS requires employers to do the rate of application for all uses of any Pesticides can enter the human body following for workers: pesticide with an REI on the label. through contact with the skin, inhala- Records must be made before the tion, or ingestion. For protection from 1. Notify workers about applications application and kept for 30 days exposure to pesticides on your skin, read and areas under REI. Employers following the REI. This form satisfies the PPE statement on the label. Wear must post written signs that meet both WPS and the Federal Record the recommended chemically resistant EPA standards. Some products may Keeping Regulations. gloves and coveralls. Clean and main- require both signs and oral warnings. tain PPE according to manufacturer 2. Keep workers out of areas where directions. Check regularly for signs of pesticides are being applied. wear and tear. The minimum PPE Safe Handling of required for any pesticide application is 3. Keep workers out of areas under Pesticides a long-sleeved shirt and long-legged REI, except for early-entry excep- pants. Of the contamination that lands tions. Pesticide labels should be read at least on a person’s body during mixing and five times: before buying a pesticide; loading, 98 percent ends up on the Mushroom producers also may have to before storing a pesticide; before mixing hands and forearms. This contamina- comply with the Occupational Safety and loading; before applying the tion is avoided easily by wearing long- and Health Administration Hazard pesticide; and before disposing of the sleeved shirts and gloves. For protection Communication Standard. This law empty container and/or unwanted from breathing pesticide fumes and requires employers to make Material product. vapors, read the PPE statement on the Safety Data Sheets on all hazardous label. Wear the recommended respirator chemicals in the workplace, not just Keep in mind that the label is the law! It and clean and maintain it regularly. pesticides, available to employees. is a legal document. If label directions Have a respirator fit-test each season. To are not followed, the law has been protect against ingesting pesticide, never The Federal Record Keeping Regula- broken—an action that may warrant eat, smoke, or drink while handling tions require that private applicators fines and/or penalties. The label tells pesticides. Wear a face shield while keep application records of restricted- how toxic the pesticide is, what PPE to mixing and loading to prevent danger- use pesticides. Records must include the wear, and how to protect the public ous splashes. pesticide name, EPA registration from exposure and the environment number, total amount of active ingredi- from contamination. The label also tells If transporting pesticides from the ent applied, size of area treated, com- how, where, and when to apply the dealer to your place of business, keep modity, location of application, and product and what pests are controlled. the pesticides in the bed of a pickup certified applicator’s name and number. truck. Never carry pesticides in the Records must be made within 14 days Probably the most important words on passenger compartment of a vehicle. Tie of the application and kept for 2 years the label are the signal words, which the containers down and carry an in an easily retrievable format. They indicate how toxic the product is to the emergency spill kit. Long-term storage must be surrendered to medical person- applicator: Caution—least toxic; of containers should be in a locked, dry, nel upon request. Pennsylvania requires Warning—moderately toxic; Danger— well-ventilated facility that is free from these records to be kept for 3 years. most toxic. Remember this equation: temperature extremes. A sign on the Risk = Toxicity x Exposure. Your risk of door should warn that pesticides are The Worker Protection Standards cover being poisoned by a pesticide is equal to stored inside. In case of fire, emergency both restricted-use and general-use the toxicity of the product times your personnel need to know that toxic pesticides. They require producers to exposure to the product. Never use a fumes may come from this room. The keep application information in a product with a danger signal word if a floor of the storage facility should be central location where workers normally product with a warning or caution made of sealed concrete for easy congregate. Information must include signal word will get the job done just as decontamination after spills. Any the pesticide name, EPA registration well. The product with the danger shelving should be of stainless steel, as number, time of application, and re- signal word will not kill the pest any wooden shelves will soak up spills from entry date and time. Pennsylvania also faster, but it will be more hazardous to open containers. Fumes from such spills requires records of the formulation and the applicator’s health.

45 will continue to contaminate any visitor While mixing and loading, wear the In the case of a pesticide emergency, to the room. correct PPE. Connect a backflow read the information posted at the preventer to the hose to prevent back- central facility, which will include the Place open containers in secondary siphoning and contamination of the location of the nearest emergency containers. Disposable “turkey roasters” water supply. During the application facility. Clipboards with emergency from a department store work well. procedure, make sure that no workers procedures should be kept in pesticide Never keep food, feed, seed, or business are in the area. Wear the label-required storage facilities and in mixing/loading products in the pesticide storage facility. PPE for the application, and let some- areas. All workers should be familiar Absorbent materials like stationary and one know you are working with with, and review often, the information paper towels will absorb pesticide fumes pesticides in case of an accident. Clean posted on the clipboards. and contaminate users repeatedly. Never the spray tank after each use or use a store PPE in the pesticide storage dedicated sprayer. facility for the same reason. Keep a spill cleanup kit handy: broom, dust pan, After the application, triple rinse or jet mop, bucket, bleach and lye (for rinse empty containers. Take the decontamination), and spill control containers to a pesticide container products. Cat litter will soak up a spill chipping facility to recycle them. Check easily. Newer products made of gel with the appropriate state department flakes will pick up the spill and allow of agriculture to determine availability you to transfer it to the spray tank for of chipping facilities. Unwanted application. (Gel flakes will not clog pesticide can be disposed of by use on- applicator nozzles.) This means that it is site, or a hazardous waste contractor not necessary to dispose of a valuable may be hired to remove the unwanted pesticide or hire a hazardous waste product. Avoid the problem of un- contractor to clean up a spill. wanted pesticide. Buy only what can be used in one season or less. Stockpiling Proper calibration of application of inventory is not recommended, equipment will save money by avoiding because the EPA may cancel a product product overuse. In addition, calibra- before one that is in storage is used. tion prevents loss of commodity from Likewise, the manufacturer may excess pesticide residue. Fill a spray tank produce a better pesticide than an with water and put the nozzle in a inventoried chemical, or stored products bucket to collect the spray. Run the may become obsolete on a particular sprayer for the amount of time it would farm because of a change in the farm’s take to spray one bed. Measure the pest complex. There are many reasons amount of spray collected in the bucket. for buying pesticides in small quantities If this is more pesticide than the label and using stock quickly, not the least of recommends for one bed, it will be which is that improper storage and necessary to move the spray wand faster disposal of empty containers and over the bed. If the amount collected in unwanted product can contaminate the the bucket is less than what the label environment. recommends for one bed, it will be necessary to spend more time applying Following pesticide application, shower the product to ensure adequate cover- and put on clean clothing. Wash age. applicator clothing on-site, or use disposable PPE. If clothing must be taken home, wash it separately from family wash.

46 C. Pest Species Biology and Control

monitor the number of female flies Sciarid Flies entering the house and emerging from 1. Arthropod Pests the compost/casing during the crop. The major insect pest of mushrooms in Males, on the other hand, are found Clifford Keil North America is the sciarid fly, primarily on the surface of the casing Lycoriella mali. These flies are small searching for newly emerged females to 1 black insects about ⁄4 inch (3–5 mm) mate with. Adult flies do not actively long with long antennae and gray wings feed but may take in some water. The held folded over the back (Figure 17). immature sciarids (larvae) are translu- Females are more abundant and larger cent, white, legless maggots that range 1 1 than males. Female sciarids have a in length from ⁄8 to ⁄4 of an inch (1–8 pointed abdomen that is frequently mm). The head is large and dark with swollen with eggs, while males have powerful chewing mouthparts that prominent claspers on the end of their distinguish sciarid larvae from other abdomen that are used in mating. insect larvae that might be found in Females are attracted to lights and mushroom production houses. The frequently can be seen on backlit larvae are the feeding stage in the life windows, vents, picking lights, and cycle of this fly. black light traps. This attraction to light provides the grower with a means to

Figure 17. Sciarid fly and larva.

47 Sciarids like L. mali are found naturally clumps. The larvae hatch from the eggs There is evidence that the timing of the in cool shaded woods and areas of dense after about 4–6 days at regular compost life cycle for L. mali may change with vegetation. The females seek out spots temperatures (75–80°F, 24–27°C). The development on different strains of to lay their eggs where fungi have just first instar larvae begin feeding immedi- Agaricus bisporus, different species of begun to colonize the substrate. ately on mycelium and the compost Agaricus (e.g. A. blazei or A. bitorquis), Accordingly, L. mali females invade itself. The larvae go through 4 instars to or different species of mushroom 1 mushroom production houses as the reach their maximum size of ⁄4 inch, (Pleurotus or Lentinula). There have compost cools down after peak heating shedding their integument at each molt been reports that L. mali populations and the mesophilic fungi in the com- to get larger. This is a vulnerable stage that have become resistant to certain post begin to grow. This invasion in the life cycle, and some insect growth pesticides may take longer to complete continues during spawning. It is regulators are active only on molting development. essential to protect the crop by placing larvae. The larvae are voracious feeders plastic on the bed surfaces and keeping and attempt to eat anything they find in The feeding of larvae in the first the doors and other entry points closed their jaws as they move through the generation probably does little damage during this period. Running black light compost and casing. This includes other to the crop. The exception to this rule traps during this period is a good way to sciarid larvae (they are cannibals) and would be in situations where Tricho- assess the tightness of fly exclusion other insect larvae they might encounter derma green mold is prevalent. In this measures and also pinpoint the time of in the compost and casing. They prefer case, it is likely that even small infesta- invasion. Female sciarids are capable of to feed on developing mycelium and tions of flies can significantly magnify finding cracks to enter voids in block compost as opposed to a dense mycelial the damage from this disease. Very high walls to find entry into rooms with mat. It is hard for the larvae to feed on numbers of larvae feeding in the running spawn. They are very tenacious. mycelium in fully spawn-run compost, compost during spawn run also can Adult L. mali prefer cool temperatures as it is water repellant and studded with inhibit fruit body production through and are most active when outdoor calcium oxalate crystals. destruction of the compost and the mycelium. In most situations, crop temperatures are between 50°F (10°C) About 21 days after the eggs were laid, damage and loss of yield and quality and 75°F (24°C). Consequently, the threat of infestation is greatest from the larvae transform into pupae, the result from the ability of the adults to March to July and September through transition between the larvae and the mechanically spread mushroom diseases late November in most of North adult. This stage is inactive and does not such as Trichoderma, Verticillium America. This threat is diminished feed. Many times, the larva will spin a fungicola, and Pseudomonas tolaasii. The during the hottest part of the summer, silk chamber to protect itself during feeding of the second generation larvae especially under dry conditions and pupation. Pupation generally lasts about also can be extensive and can result in after three successive frosts. a week. The males typically emerge 1–2 yield loss through degradation of the days before their sisters. Because there is compost and casing, and destruction of Once inside a growing room, a female a narrow window for oviposition during mycelium and fruit body primordia in L. mali typically will land on compost cooldown and spawning, the first the casing. In severe infestations, larvae close to the point of entry to lay her generation of L. mali emerges as adults can tunnel up into the stipe, resulting in eggs. Depending on how well fed she very synchronously just before first the condition referred to as “black was as a larva, she may lay up to 150 break. This synchronous development stem,” which renders the mushrooms eggs. Female L. mali can be very allows the grower to apply insect growth unmarketable. The potential for crop discriminating in choosing a spot for regulators and biological controls such damage through reduced yield and oviposition. They can detect residues of as nematodes to the most susceptible quality is significant with this pest. Dimilin and avoid laying eggs on life stages of the insect by timing Growers must be continuously vigilant substrate with this pesticide. They also development from the peak invasion on to avoid crop damage from this insect can detect the presence of Trichoderma light traps. The complete life cycle pest. and will lay their eggs preferentially in requires about 28 days at normal areas contaminated with this fungus. compost temperatures. A peak of 1 The eggs are small, ⁄16 inch long, emergence usually can be seen for the translucent and white, and oval. They second generation, but it is less distinct. may be laid as singles or in large

48 Female phorids enter the growing room Because the larvae feed selectively, they Phorid Flies and lay about 50 eggs in areas where are not capable of causing the kind of there is fresh mycelia growth. The larvae damage that sciarids do as larvae. A pest of secondary importance in hatch after several days and begin Significantly more phorid larvae can be North America is the phorid fly, feeding. They pass through three to four tolerated—perhaps as much as 50 to Megaselia halterata. These flies are small, instars. They are more sensitive to 100 times more than sciarids—before 1 variations in compost and casing economic damage can occur to the crop. ⁄8 inch (2–3 mm) in length, with a humpback appearance and very small temperature than sciarids, and the Phorid adults are very capable of antennae (Figure 18). They appear timing of the life cycle is variable. At transmitting fungal and bacterial stockier than sciarids and are very warm compost temperatures of 75– diseases, however, and control of the active, running and hopping erratically. 80°F (24–27°C), development from egg adults is necessary to maintain crop The males and females closely resemble to adult may require only 15 days. health. Because they are active fliers, each other. Adult phorids typically enter During cropping with lower tempera- they can be a significant irritant to the production rooms and houses later tures (60–70°F, 16–21°C) in the casing, picking crews, and control of the adults in the crop cycle than sciarids. They development may extend up to 50 days. may be necessary to maintain efficiency. 1 prefer warmer air temperatures and The larvae feed only for about ⁄3 of this drier conditions in the substrate. They period of immature development. The also can become a problem later in the remainder of the time is spent as the year, typically June and July. Conse- immobile and nonfeeding pupa. The 1 quently, infestations of M. halterata are pupae are about ⁄8 inch long and typically seen in drier areas of casing gradually turn from cream colored to after second break. The larvae are dark brown as they mature. The pupae creamy-white maggots that are no are flattened and oval in shape with 1 breathing horns at the broad head end. longer than ⁄4 inch (6 mm) when fully grown. The rear end is blunt and contains the opening of the breathing Figure 18. Phorid fly and larva. tubes. The head is pointed and the same color as the rest of the body. The mouthparts are relatively small hooks held inside the head. Phorid larvae feed only on mycelium and graze selectively.

49 Cecid larvae are legless maggots, bluntly The two orange Mycophila are not as Cecid Flies pointed at both ends. The head and the common as the white Heteropeza, but tail are not easily distinguished, except can cause significant damage. They have A variety of other species of flies can be by the direction of travel. White larvae a slightly shorter life cycle and therefore encountered in mushroom houses. The typically are the species Heteropeza can develop damaging population levels most potentially damaging are cecid pygmaea, while orange larvae are in the rapidly. However, their orange color flies (Figure 19). Three species have genus Mycophila, either speyeri or makes them more conspicuous, and been identified as pest species in the barnesi. Heteropeza pygmaea is probably growers typically notice them before United States. These three species are the most commonly encountered cecid large populations are attained. rarely seen as adult flies, because under in mushrooms and has been reported Cecid larvae have the potential of most conditions larvae become “mother from Agaricus as well as other species, feeding on mycelium within wooden larvae” that give birth directly to 10–30 particularly Pleurotus. The small, sticky structures inside growing rooms. daughter larvae. These species usually larvae are spread by workers and on Because the wood offers some insulation do not become a pupa and subsequent tools and equipment. Initial entry to the from the heat of cookouts, they may adult that must mate before laying eggs. growing room may be by transport of survive the high temperatures and infest Reproduction is accomplished without infested peat or substrate, movement the next crop. Direct treatment of wood mating and gives rise to daughter larvae with personnel, or through the rare with insecticides and fungicides may be directly. This is termed paedogenic flying adult. Small infestations may not necessary to reduce between-crop parthenogenesis. When conditions are be readily apparent at first. The larvae survivors if there are high populations of optimal, this method of reproduction feed on the mycelium as well as on the cecids on the farm. can result in very rapid multiplication of stipe and gills of mature mushrooms. If this pest, leading to astronomical large populations develop, the larvae numbers of larvae, tens of thousands per may mass together on the floor and square foot. disperse in large groups. Larvae also can be found on mature mushroom caps packed for market. This species has the potential to significantly reduce yield when it becomes established on a farm.

Figure 19. Cecid fly and larvae.

50 Other species of flies may indicate that Other Flies anaerobic conditions may have devel- oped at some place on the farm or in A number of other species of flies may growing rooms. These flies include be noticed by alert growers, especially black scavenger flies (sepsids), moth flies on light traps. Most of these are (psychodids), and small dung flies incidental and may indicate that certain (spherocerids). conditions can be found in growing rooms that require attention. Occasion- ally, they indicate the presence of a new pest on the farm. When in doubt about the identity of insects found on the farm, do not hesitate to submit samples for identification.

Flies that resemble a large phorid with prominent red eyes are probably fruit flies in the genus Drosophila. The term “fruit fly” is a misnomer for this group, as the larvae all feed on fungi of one sort or another, in some cases on rotting fruit. In the wild, larvae of these flies can be found feeding on mature sporophores in great numbers. These larvae resemble small house fly maggots in that they have a pointed head with small mouth hooks and a blunt rear end with breathing tubes. If we think of sciarids and phorids as feeding on the early stages of mycelial growth in the life cycle of a fungus, we can think of Drosophila as feeding late in the life cycle. If you see significant numbers of Drosophila adults, there are probably areas in the growing room with large, over-mature mushrooms. This can be a problem particularly in portobello production if large, nonmarketable mushrooms are not picked off the bed promptly. The danger here is that if large populations develop, eggs may be laid on mushrooms packed for sale. If the eggs hatch and larvae begin feeding during transit, storage, and display in the retail store, consumers may purchase mushrooms with maggots in the cap.

51 C. Pest Species Biology and Control

2. Fungal Introduction Verticillium Diseases Pathogens There are many fungal pathogens of mushrooms, but only a few of them Common names: Phillip S. Coles currently affect commercial mushroom Verticillium disease, Verticillium William Barber farms. Some of these are true pathogens spot, brown spot, fungus spot, dry attacking the mushroom mycelium, bubble while others can simply outcompete Scientific name: mushroom mycelium growth. Fungal Verticillium fungicola pathogens can either affect the quality of the product, reduce production, or Outdated names: both. But all of them reduce the total Verticillium malthousei, return of a crop, often significantly. Acrostalagmus fungicola, Cepha- Many control methods, such as sanita- losporium constantini tion, are useful for all of the diseases. There also are control measures specific Perfect stage: to each disease. unknown

Verticillium is one of the most signifi- cant diseases of commercial Agaricus production. It is endemic on many mushroom farms and can cause substan- tial yield reduction. It can occur in nature in addition to cycling within a mushroom farm, traveling from older to newer growing rooms.

52 Identification Infections on the mushroom stem will More significant infections cause serious cause exterior cells to die. Because the deformation of the sporocarps, which Infection takes on a variety of forms and exterior cells no longer will grow while will appear as large, formless, puffball- has various symptoms, from small the noninfected cells continue to like masses. The cap becomes indistin- spotting on the surface of a mushroom elongate, the mushroom will bend guishable from the stem (Figure 20). cap to a complete infection of the towards its infected side. Further, the Growers commonly refer to this fruiting body so that it is unrecogniz- dead cells will split and crack, causing a symptom as “dry bubble.” Its expression able as a mushroom. Appearance will “blow out” (stipe blast) on the side of requires early infection by Verticillium depend on the timing of infection and the mushroom stem. An infection on spores. The Verticillium spores must the number of spores. the stem also can be expressed as a have infected the pins early enough, and The first symptom group is spotting, a streak along the length of the stem. with enough spores, to have time to superficial infection causing necrotic completely take over the growth of the lesions on the cap of the mushroom. pin. Bubbles will be covered with the These spots will enlarge and coalesce as gray fuzzy bloom of the Verticillium the mushroom enlarges. This easily can conidiophores. be confused with bacterial blotch or Trichoderma spot. Spotting is the result Figure 20. Verticillium in the dry bubble stage. of late infections of Verticillium. The mushroom already had developed when the infection occurred, and the patho- gen only had time to infect the mush- room superficially.

A simple way to determine which organism is causing spotting is to place infected mushrooms into a sealed plastic container with a few moistened paper towels. The water in the towels will keep the humidity of the chamber high, and the causal agent will grow out from the mushroom tissue. If the infection is bacterial, the color of the spots will not change. Trichoderma spot, on the other hand, will turn green when the fungus sporulates, and Verticillium will turn the mushroom surface gray and give it a fuzzy texture.

A very localized infection on the mushroom cap can be expressed as a “harelip.” The infection kills the cells in a specific area, preventing growth. Then, while the other cells of the cap continue to grow, expansion occurs everywhere except within the infected area. This causes the pinched area, or harelip. The dead area of the sporocarp will appear gray and leathery.

53 Figure 21. Verticillium spot. nozzle or hose is used at the end of a crop and then moved to an earlier stage, infection can result. Harvesting baskets traveling to and from a processor also can be a source of inoculum if the baskets are delivered from an infected growing area to the processing plant and are returned to the farm—or delivered to another farm—where they might infect a previously clean growing area.

Verticillium can be spread on air currents. Spores will stick to dust particles and can enter a growing room through the ventilation systems. Dust can settle on equipment or casing materials en route to a room. Spores also can travel on airborne mites, regardless of whether or not the mites are living.

The initial infection may come from one of many sources, but once inside a Biology spread to uninfected sites by many room, the infection can spread very different modes. The spores are very Verticillium spot (Figure 21) takes about quickly. This is due to the high repro- sticky and can be carried by anything to 7 days to produce visual symptoms. If ductive capability of the Verticillium which they are able to stick. This there are visible lesions, stipe blast, or organism, which can produce 30 includes, but is not limited to, person- other superficial mushroom deformities, million spores per hour. Tests on petri nel and their clothing, mushroom flies, it can be concluded that Verticillium plates have shown that, after touching mites, and rodents. Flies are particularly spores infected that mushroom about 7 one bubble that is sporulating, a finger problematic vectors, since they actively days before the appearance of symp- can touch eight more petri plates and are trying to leave older growing rooms. toms. For an actual bubble to appear, cause infections on every plate. There- Flies likely will pick up Verticillium the infection requires a 10- to 14-day fore, anything contacting a sporulating spores in the older rooms and spread the incubation period. Therefore, if the bubble can infect many potential sites. infection to new rooms. In addition, mushroom pin already is formed at the High fly populations are very effective they can carry mites that in turn can time of infection, there will be only at spreading an infection throughout a transport Verticillium spores. superficial markings on the mushroom. room. Water hitting an infected site can If the infection begins soon after casing, Once the mites leave the bodies of the pick up spores and splash them onto dry bubbles will be formed. flies, they will spread spores while other mushrooms, infecting them with moving throughout the room. Rodent Verticillium. Harvesters and their Verticillium needs the developing fur is an excellent carrier for the sticky equipment will spread an infection sporophore to manifest symptoms. The spores, and the tendency for mice and quickly throughout a growing room, as mycelium germinating from the rats to bore into mushroom beds in well as from room to room. Verticillium spores will grow into the search of spawn grains can expose a lot mushroom tissue, parasitizing and High spore loads can develop on the of material to infection. Equipment can deforming it. Mushroom mycelium floors and other infection sites, increas- be a source of inoculum, especially alone will show no symptoms of ing the possibility of spores being equipment that is moved from dirty Verticillium. picked up by a vectoring agent. Dead areas to clean areas. A good example is mushrooms also can be reservoirs for watering or spraying equipment. Verticillium infections are caused by inoculum. spores and mycelium transported or Watering and spraying are done throughout the crop, and if a watering

54 Control gravel roads. Filter air to exclude spores and anything that may be carrying Monitoring Verticillium control depends primarily them, such as flies or mites. (See on eliminating spores through sanita- The most useful method of monitoring Chapter II.A.1, Exclusion.) Control fly tion and control of vectoring agents. All Verticillium is to count the number of and mite populations and their move- equipment should be kept in dedicated bubbles in a growing room. By mapping ments into new growing areas. (See storage areas. Equipment and personnel the number and location of the bubbles, Chapter II.C.1, Arthropod Pests.) you can detect patterns. Improperly from dirty areas never should be allowed sanitized casing equipment may show to enter clean areas, and personnel and Bubbles can be destroyed with salt. The itself in a high concentration of bubbles equipment from clean areas never best method is to put salt into a plastic in the area where the casing crew starts. should be allowed into dirty areas. If drinking cup, then cover the bubble High bubble counts in rooms having hoses or spray apparatus, for example, with the cup and salt (Figure 22). The the highest incoming fly populations must be moved between clean and dirty salt will desiccate the bubble, preventing could indicate spores coming in with areas, they should be moved from further mycelium growth, and the flies. High bubble populations near newest to oldest rooms, then sanitized plastic cup will prevent the spores from doors might suggest that dust is before they are returned to new rooms. spreading. Bubbles can be physically entering through doorways or that there (See “Sanitation” in Chapter II.A.2, removed from the growing room. This are possible ventilation problems. Cultural Control.) is often done in an alcohol solution. The procedure is risky, however, since Harvesters must be trained to recognize Understanding the timing of Verticil- the bubble is disturbed and spores and not touch bubbles. More impor- lium disease is essential for controlling might be released. Worse yet, the person tantly, employees must be taught the it. The time when a specific symptom removing the bubbles can become a importance of cleanliness, particularly if manifests itself is a good indication of disease vector. when the infection occurred. If bubbles they work in clean areas. Control dust appear on first break, for instance, there by paving roads or by oiling or watering probably was a breakdown in sanitation in the peat moss preparation, the casing Figure 22. Salt will kill the Verticillium, while the cup will prevent the spread of operation, or an early stage of case spores. growing, since there is a 10- to 14-day incubation period for bubble develop- ment. If bubbles do not occur until the last break, it is likely that spores are entering once harvesting has begun, either on harvesters or harvesting equipment.

55 Fungicides have been, and most likely from their microscopic characteristics, will continue to be, available for the Trichoderma Green Mold but to date there is still no satisfactory control of Verticillium. There is, classification of species in Trichoderma. however, a special difficulty with trying In addition, there are many different to develop a fungicide for a fungal Common name: strains or races in the various species. pathogen of a crop that is itself a green mold They can vary in aggressiveness, fungus. Very often the fungicide will resistance to heat or pesticides, and in a have a toxic effect on mushroom Scientific name: variety of other ways. growth. This must be weighed against Trichoderma harzianum the benefit of Verticillium control, since Trichoderma species are asexual fungi Perfect stage: that propagate through vegetative some mushroom production could be unknown lost. Also, since pesticides that are the growth and production of asexual spores least deleterious to the mushroom crop (conidia). The conidia are spread easily by various means. Trichoderma also can must be used against Verticillium, the Trichoderma harzianum is a relatively fungicide’s mode of action against dry have a sexual stage in which its appear- new disease of commercial mushroom ance is changed so substantially that it bubble must be targeted to one of the production. It was first encountered in few things that is different about originally was classified incorrectly as Ireland and the UK in 1985. During belonging to the genus Hypocrea. Verticillium and Agaricus. Since mush- the 1985–1986 growing season, the rooms and Verticillium are very similar ensuing epidemic caused losses esti- The members of the genus Trichoderma from a pesticide’s point of view, any mated at one million monetary pounds have a considerable arsenal of “chemical differences between the two that are ($l.5 million U.S.). Through 1990, weapons” that are produced in the form exploited by a pesticide’s mode of action losses were estimated to be between 3 of antibiotics and other toxins that would be small, and there would be a and 4 million pounds ($4.5–6.0 million strongly inhibit the growth of other stronger propensity toward the develop- U.S.). In 1990, it appeared in British organisms. Furthermore, some species ment of resistance than normally occurs Columbia, and in the Ontario area in are capable of parasiticism on the in most pest species. Therefore, pesti- 1992. In 1993, it reached the Berks mycelium of other fungi. Its aggressive- cides should be used sparingly, only County growing area of Pennsylvania ness makes it useful as a biological when needed, and according to eco- and, in 1994, Chester County, Pennsyl- control agent against fungal pathogens nomic thresholds (See Section I.B). vania. Since then, it has become of green plants. This same aggressive- In some instances, despite whatever endemic in Pennsylvania. ness, however, makes it a serious combination of control measures are pathogen in commercial mushroom Aggressive strains of Trichoderma production. used, Verticillium can run rampant harzianum have been associated with throughout a growing room. Sometimes the commercial production of Agaricus It is now possible to isolate different it is possible for every developing bisporus. In the UK, the aggressive form species and strains through Polymerase sporophore to be expressed as a bubble. is known as “Th2.” In the U.S. and Chain Reaction (PCR), but when first In this extreme example, there is no Canada, “Th4” is the dominant encountered, green mold samples had to point in continuing the crop, especially aggressive strain. These aggressive strains be identified through microscopic if no harvestable mushrooms are being have been found only on mushroom examination that was very time- produced. The room will have become farms and only recently. consuming and always suspect as to an incubator for Verticillium spores and accuracy. PCR examination also has most likely will be producing flies that The genus Trichoderma includes many shown that green mold is not a new will further spread the spores and those common soil-inhabiting fungi and strain of Trichoderma that mutated from of other molds. Trying to save old crops decaying organisms associated with an existing form, nor is it one of many with this level of infestation will result wood and decaying vegetation. In strains developed for biological controls in the continuation of the infection nature, it has an important role as a on green plants. It probably has been cycle. Steam the room early and decomposer. Trichoderma is a very around for millions of years, and eliminate this potential source of complex genus, and not until 1969 did changes in cultural practices made it inoculum. Rafi properly clarify the taxonomy. very successful in mushroom houses. Nine species aggregates were identified

56 Beyond mushroom farming, it is very Figure 23. Trichoderma mycelium, showing dark green color. rare.

Trichoderma mycelium grows on compost and competes aggressively with mushroom mycelium. Microscopic observation of the interaction between Trichoderma and mushroom mycelium does not show any obvious pathogenic- ity. This has lead to debate about whether Trichoderma green mold is a fungal pathogen or a competitor.

Identification

Trichoderma mycelium is gray in the beginning and then changes to white, becoming very dense. After fruiting, its spores turn it a dark green (Figure 23). There are many other types of molds that also are green and associated with mushroom compost, including Figure 24. Widespread green mold infestation. Gliocladium, Cladosorium, Asperigillus, Penicilium, and Chaetonium. Care must be taken not to confuse them with green mold. There also are other species and varieties of Trichoderma that will not cause the disease, and only through close taxonomic examination or through PCR can they be differentiated. However, if green mold progresses rapidly across the growing surface (Figure 24), it can be assumed to be one of the aggressive varieties of Trichoderma green mold.

Pygmy mites often are associated with green mold infestations, though this is not always the case. They also can occur in the presence of other types of fungi.

57 Biology is not enough. Grogan showed that it is Control possible to get an infection from less To infest a mushroom crop, Trichoderma Control begins in Phase I and Phase II than 100 spores, though normally more first must have its spores introduced. composting, where the number of are needed. For experimental purposes, The spores are contained in a sticky spores in the compost must be mini- at least 9 million spores are used in each matrix that can attach to many different mized. Any green mold spores that may inoculation. surfaces. Consequently, many of the get into the compost during these stages traditional pathways of other types of Once germinated, the green mold must be destroyed to prevent germina- fungi also apply to green mold. The mycelium will move quickly into tion in the growing rooms after the spores can adhere themselves to employ- compost and colonize it. Consequently, room is planted. ees and their clothing, as well as to mushroom mycelium no longer will be Minimize potential inoculum sources by equipment used on the mushroom able to grow there. The green mold then not allowing unpasteurized materials farm. Rodents can carry spores, and will move into compost already colo- from harvesting, such as mushroom spores can travel on flies or on mites nized by mushroom mycelium and will trimmings, onto the compost wharf carried by flies. (Mites are excellent spread across an entire growing surface. vectors because they have specialized where green mold spores could collect organs known as sporangia, which are Monitoring in the leachate pond. It is better to used to spread fungal spores.) Mush- remove all trimmings from the farm site Use the Verticillium mapping technique if possible. room trimmings can be a reservoir for to monitor green mold; i.e., count the spores, and the practice of putting number of squares infected with green To eradicate spores that may get into trimmings in compost can add to mold in a growing room and map the the compost, cross-mix during Phase I inoculum sources. If post-harvest and number and location of the infections. so that all the material is exposed to the Phase II pasteurization are insufficient, By noting the number and location, you highest composting temperatures green mold spores can survive to infest a can detect patterns. Improperly sani- possible. Control moisture to ensure new crop. tized spawning equipment may show that the maximum amount of compost It is not enough for spores simply to be itself if the highest concentration of reaches these temperatures. Formulate present; they must exist in sufficient green mold is in the area where the so there is a distinct ammonia odor at numbers and correct conditions must spawning crew starts. High green mold the end of Phase I. The ammonia will prevail. No specific compost or environ- counts in rooms or in areas of a room help to degrade the exterior of the spore mental conditions have been found to having the highest incoming fly coat. populations could indicate that spores be associated consistently with green Phase II pasteurization must be com- mold development. It has been shown are coming in with flies. High green mold populations near doors could plete. Pasteurize at 140°F (60°C) for that a carbohydrate source is necessary two hours. Beds must be filled uni- for spore germination. Spawn grains indicate that dust is entering through doorways or that there are possible formly to ensure that all areas attain this serve the carbohydrate requirement very temperature. well if they are fresh (the mycelium has ventilation problems. not yet grown into the compost) and if The time at which a specific symptom Disease control depends primarily on the green mold spores are within one manifests itself is a good indication of eliminating spores through sanitation centimeter of the grain. Green mold, how severe the infections were at and control of vectoring agents. therefore, will not germinate in fully spawning. If no green mold is detected Sanitation at spawning is more impor- colonized compost, where the mush- except for a few spots at the end of the tant to control of green mold than, for room mycelium protects the grain from crop, the amount of inoculum probably instance, control of Verticillium, which the disease. Green mold spores intro- was low. If it is seen when the plastic is is more dependent on control after duced at casing will not germinate for pulled at spawn run, there was a serious casing. Harvesting and overall farm the same reason. Also, a minimum infestation. sanitation are important for control of number of spores are required. Theo- both organisms. All equipment should retically, only one spore is needed to be kept in dedicated storage areas. start a green mold infection; but, as is Equipment and personnel from dirty true with most types of fungi, one spore areas never should be allowed to enter

58 clean areas, and personnel and equip- spawn. First, spawn must be kept clean. ment from clean areas never should be In order to be mixed with a fungicide, Dactylium Diseases allowed into dirty areas. If hoses or spawn must be removed from its spray apparatus, for example, must be original packaging, exposing it to moved between clean and dirty areas, possible contamination. This could Common Names: they should be moved from newest to result in a worse green mold infection cobweb mold, Dactylium mildew, oldest rooms, then sanitized before than if no fungicide had been applied. soft mildew, soft decay being returned to new rooms. (See more Therefore, sanitation is of the utmost Scientific Name: on sanitation in Chapter II.A.2.) importance during this operation. Dactylium, cladobotryum Control dust by paving roads or oiling Second, tumbling the spawn in a mixer or watering gravel roads. Filter air to Outdated names: damages some of the mushroom exclude spores and anything that may Dactylium dendroides, Nectria mycelium on the spawn grains and can be carrying them such as flies or mites. albertinii, Nectria rosella, reduce its vigor. Mix the grains as gently (See more on exclusion in Chapter Cladobotyium dendroides II.A.1.) To further reduce green mold as possible. Once it is mixed with the spore spread, take the additional step of fungicide, spawn usually is stored in a larger bag than the original packaging. using separate cafeterias and break Identification rooms for employees working in areas Therefore, care must be taken to other than harvesting. This also will prevent overheating of the spawn before Dactylium mildew, or cobweb mold, can help with other types of pathogens. it is applied to the compost. Of course, be recognized by its wefty, cotton-like Employees working in the spawning pesticide labels must be followed at all mycelium. The mycelium will cover the area should be issued new uniforms times. surface of the casing as well as the daily. Fungicide applications should be surface of mushrooms and mushroom limited to avoid resistance development. pins. The mycelium is usually white, Areas infested with green mold can be but can be gray and often turns pink or controlled with salt or hydrated lime by They should be used as a “last resort” when green mold infestation is out of yellow with age. Infected mushrooms sprinkling the infected areas with either develop a soft, wet rot. material. The salt or lime should extend control. Sanitation is the only way to at least 8 inches from the edge of the control green mold in the long term, Cobweb mold is a relatively minor visible growth, since adjoining casing and once the disease is brought under disease of mushrooms, but because of its can harbor the mycelium and soon be control, the use of fungicides must be ability to grow quickly, it can spread producing spores. If mycelium appears stopped to reduce the chance of over many mushrooms. If left un- on the surface of the compost before development of resistant green mold checked, widespread mildew can result casing, spray the area with a 1,000-ppm strains. (See more on resistance manage- in unsalable mushrooms and eventual chlorine spray, again extending the ment in Section I.A and Chapter significant yield loss. treatment 8 inches beyond the II.A.4.) Biology infection’s visible edge. As with Verticillium, if green mold gets Cobweb mold occurs only on the casing Existing chemical pesticides essentially out of control, it is better to steam off layer and cannot grow in the compost. are ineffective on green mold mycelium the room early rather than risk the Therefore, infection must take place once it is growing actively in compost or spread of infection to new rooms. after casing. Symptoms can occur before casing. However, it has been shown that Reducing the amount of inoculum will first break, but they usually appear later some types of fungicides applied to yield benefits to future crops that are in the crop. Dactylium may thrive in the spawn grains will provide limited greater than the benefits that might be controlled environment of a mushroom protection to the grains and prevent reaped from the few mushrooms that facility, but it also can survive in wild green mold spores from germinating. could be salvaged. Post-harvest must be mushrooms or in soil. Inoculum can Tu mbling the spawn with the fungicide adequate. come from outside sources surrounding mixed with a carrier such as gypsum a mushroom farm or from older rooms coats the grains. Great care must be where infections have occurred. Unpas- taken when applying fungicides to the

59 teurized soil or spent mushroom cause more harm than good, for, if it is substrate used for casing can be a source done when cobweb mold is present, an of inoculum. Actually, any type of epidemic may occur because the mold’s casing can cause infection if it has rate of growth will increase faster than become contaminated. Further, spores that of the mushrooms. Maintaining the can enter a growing room through optimal temperature for mushroom ventilation or on employees or equip- growth, on the other hand, will be ment. Infection often begins on dead detrimental to the growth of cobweb material left on the casing surface. Dead mold. fruiting bodies or the stumps trimmed from mushrooms can be a food source Since high humidity promotes the for germinating spores. From there, the growth of cobweb mold, it is very infection can spread to the casing layer, susceptible to control by desiccation if covering it and any mushrooms or pins growing room relative humidity is in its path. Infections can appear lowered. Maintain the room tempera- quickly and can spread rapidly. Trash ture below 65°F (18°C) and the relative left on beds, high relative humidity, and humidity below 92 percent, and the high air temperatures are very conducive growth of cobweb mold will be inhib- to cobweb mold’s growth. ited.

Control Chemicals also may be used to control cobweb mold, though presently there Cultural controls, especially sanitation are no materials registered specifically and exclusion, are the best way to for it. Some fungicides applied for other control cobweb mold. Casing areas types of pathogens such as Verticillium must be kept clean and sanitized. have the unintended but beneficial Casing material must be loaded into effect of controlling cobweb mold. sanitized trucks and covered to prevent contamination during transport to growing rooms. All equipment used for casing must be cleaned and sanitized. Casing employees must be clean and wearing laundered clothing each day. Once the casing material is safely inside the room, the air must be filtered to ensure cobweb spores do not enter the room (see Chapter II.A.1, Exclusion). Beds must be kept clear of trash such as stumps or dead mushrooms, where infections can start.

Environmental control is the key to preventing the spread of existing infections, since cobweb mold needs both high humidity and high tempera- tures to spread. Often, growers will raise a growing room’s temperature to accelerate mushroom growth. A grower may be trying to outpace the growth of a pathogen or trying to complete a break on schedule. This practice can

60 C. Pest Species Biology and Control

Introduction Weed Molds 3. Weed and Indicator Molds Weed molds may be defined as molds Lipstick Mold that grow in competition or in associa- tion with the mushroom mycelium. David M. Beyer Common Names: These fungi compete for nutrients and lipstick, red lipstick may have a negative influence on the growth and nutrient uptake by Agaricus Scientific Name: bisporus; however, they are not known Sporendonema purptirescens pathogens. Some weed molds may grow in properly prepared compost for Outdated Name: supporting the mushroom’s growth, Geotrichuin candidutti, while others may not grow unless the Oosporum sp. mushroom mycelium is present. The range of effect that weed molds may have on the mushroom mycelium is broad. Lipstick mold may occur in compost during spawn run or in the casing Indicator mold are fungi that grow in during cropping. At first, this mold is compost that has not been selectively hard to distinguish from spawn growth, prepared for A. bisporus. Growth of as it first appears in spawned compost as these molds may suggest a nutritional a white crystalline-like mold. Growth imbalance in the compost. Indicator begins as small white colonies, previ- molds will grow only in compost that ously referred to as “frost on a wind- has specific nutrient conditions that shield” or “small white cotton balls” on favor their development. These molds straws or casing. When developing after grow on compounds that the mush- casing, these small white balls may be room cannot use, and once that food misidentified as mushroom spawn source is depleted, these molds will stop forming into pins. The descriptive growing and usually disappear. How- lipstick color develops as the spores are ever, because compounds were available maturing. Several shades of pink, cherry to these fungi, fewer nutrients are red, and eventually orange or buff colors available to A. bisporus, and crop yield may be found (Figure 25). It has been usually is lowered. reported that lipstick in a peat moss and Some of each type of mold have little to limestone casing remains white, and its no effect on A. bisporus, while others red color will not develop. can entirely inhibit the growth of the spawn and eventually the mushrooms.

61 Figure 25. Lipstick mold causes a descriptive lipstick color as the spores are maturing. Several shades of pink, cherry red, and eventually orange or buff colors may appear.

Lipstick mold grows slowly and usually spores around a mushroom production It has been reported that the occur- remains confined to areas of the area. Poor sanitation and inadequate rence of lipstick mold would indicate compost or casing. It does not appear to post-crop steaming are possible causes that a La France virus disease might grow outward like green mold or for an increase in spores around a also be present. However, when virus mildew. The white growth of lipstick facility. occurs, lipstick mold is not always eventually may grow into uninfected present. This phenomenon suggests areas of casing, and it is able to colonize An infestation of lipstick mold may that the virus-infected and lipstick well-conditioned compost. Significant continue for several crops or cycles on a spores are spread around or intro- yield losses are associated with heavy farm. Control is achieved through a duced into an area in a similar manner. Some of the control methods compost infestations prior to casing. If complete post-crop steaming and for this mold would be similar to the mold does not become visible until adequate pasteurization during Phase II. those for LaFrance disease. third break, yield loss will be minimal. The lipstick fungus may not be a proven pathogen of the mushroom, but its Air currents can spread spores from presence indicates the need for increased It also has been suggested that the contaminated casing or spent compost sanitation and pasteurization proce- occurrence of lipstick is related to old during watering or via pickers. Heavy dures. wet poultry manure; wet, dense com- infestations usually reflect a build-up of post at filling time; or excessive use of steam during Phase II. In addition,

62 excessive nitrogen at spawning time may Cinnamon brown mold has a variety of colony becomes cinnamon-yellow be related to increased lipstick mold. color ranges, from yellow gold to golden brown, the edges will remain white. The Excess nitrogen may be a result of the brown to cinnamon brown. Cinnamon mold grows rapidly but usually disap- wet compost or excessive moisture brown mold is one of the most common pears within 10 days or by the time condensation with too much steam. In brown molds found in mushroom mushrooms are first harvested. It is these latter cases, other molds also may houses. The mold first appears as large possible that a dense infestation will be present with lipstick. Wet compost circular patches of white or gray-white retard the crop, especially first break, or lumps of wet chicken manure may aerial mycelium on the compost, casing, and cause a slight yield reduction. not be completely pasteurized, and or on bed or tray boards. This mold lipstick spores may survive. may grow on compost, but it is most The fungus, Chromelosporium fulva, is frequently seen after casing. The mold extremely common in soil and flour- Cinnamon Brown Mold starts out white, but within a few days ishes on damp wood. Under certain spores form and the color changes to conditions, it can grow into casing not light yellow or to light golden brown colonized by spawn. Areas in compost Common Names: (Figure 26). Over time, the color that overheated during spawn run, brown mold, cinnamon brown deepens to golden brown or cinnamon, virus- or Trichoderma harzianum- mold and the mold develops a granular infected areas, or areas of wet compost at fill with poor spawn growth encour- Scientific Names: appearance. As the center of the mold Chromelosporium fulva, Chromelosporium ollare Figure 26. Cinnamon brown mold starts out white, but changes color to light yellow or golden brown. Outdated Names: Botrytis crystalline, Ostrachoderma peziza

Perfect Stage: Peziza ostrachoderma (cup-shaped fruiting bodies)

63 age the growth of cinnamon brown The mold is most commonly known as Several weeks after first appearance of mold. This mold has been observed a re-colonizer of over-pasteurized casing the mold, and after the mold has growing on undistributed supplements and spent compost. The mold will grow disappeared, small cups or disk-shaped added at spawning. Improperly condi- rapidly from infested compost areas into fruiting structures may appear on the tioned compost containing green mold casing, especially in areas where spawn casing; these are the sexual phases of the often will contain cinnamon brown growth is weak or nonexistent. It will C. fulva (Peziza ostrachoderma). The mold. Widespread infestations of grow on the casing and can become cup-shaped structures have a rubbery or cinnamon brown mold may indicate obvious throughout much of the leathery texture and usually are dark either poor sanitation or wet and growing room at the same time, brown, although chartreuse and yellow improperly conditioned compost. suggesting that airborne spores landed fruiting bodies have been observed on the casing at about the same time. (Figure 27). The high humidity and warm tempera- tures following casing are ideal for growth of cinnamon brown mold.

Figure 27. The cup-shaped structures caused by cinnamon brown mold have a rubbery or leathery texture and usually are dark brown, although chartreuse and yellow fruiting bodies have been observed.

64 Sepedonium Yellow Mold The growth of Sepedonium seems to during compost pasteurization and an affect spawn growth—the mold adequate post-crop pasteurization are colonizes compost considered ideal for essential to eliminate the threat of Common Name: spawn growth. Heavy infestations of infestation. Preventing spores from yellow mold Sepedonium yellow mold are associated entering mushroom houses during Scientific Names: with poor yields, but whether this is due spawning and the spawn-running Sepedonium spp., Sepedonium to Sepedonium or to other factors is not period is essential. High-efficiency air chrysosporium known. Sepedonium spore populations filters reduce the possibility of introduc- will build up on a farm following the ing the mold into spawning areas, and appearance of yellow mold. Strict sanitary conditions should be main- Sepedonium yellow mold begins to grow temperature monitoring and control tained during spawning. as a whitish mold that eventually turns yellow with age, and produces abundant Figure 28. Yellow mold has a distinct yellow color in compost. The tremendous spores that become easily airborne. spore load of yellow mold causes clouds of “dust” when compost is disturbed. Yellow mold differs from other yellow- colored molds by the appearance of thin white mold growing in compost during the spawn run and by the tremendous spore load that develops. The spore load causes clouds of “dust” when compost is disturbed (Figure 28). The sparse white mold turns dull yellow to tan with age. Yellow mold spores can be spread to compost by air currents before or during the filling operation, during the spawning operation or spawn-running period, or because of spent compost sticking to wooden boards or trays. Spores also may survive pasteurization in compost that is not conducive to good heat conduction and does not reach adequate temperatures.

The obvious, thick-walled spores of Sepedonium are resistant to the high heat of pasteurization; therefore, they are able to survive Phase II. These spores are spherical, golden brown, large, and distinctly spiny, a characteristic that distinguishes Sepedonium from the other significant compost yellow mold, Chrysosporium. The latter causes mat and confetti diseases. Sepedonium produces smaller oval spores, but these are rarely observed in mushroom compost specimens.

65 Pythium Disease Microscopic examination and labora- Corticium Mold tory study are necessary to identify a white compost mold and confirm the Scientific Name: Common Name: presence of Pythium. Often, other Pythium hynosporum; Pythium Corticium-like (identity not oligandrum diseases or improper cultural practices certain) cause spotty mushroom production.

Outdated Name: Little information is available on the life Pythium artotrogus Corticium mold is found in compost, history of this fungus and the mecha- on casing, or on the woodwork in nisms by which it spreads throughout a growing rooms. This flat-growing gray- mushroom production area. Pythium Pythium is an antagonistic, potentially white mold is found on straws or wood spores are large and thick-walled, and pathogenic fungus infrequently isolated in mushroom houses. It appears to grow may survive various heat and moisture from mushroom compost. The fungus from within beds or tray boards, treatments. It has been reported that has the potential to cause yield loss, uprights, cross pieces, and other wood they are resistant to heat and drought. because spawn will not grow in areas structures. When the mold grows on Viable spores have been recovered from colonized by Pythium. casing, it looks granular like salt. Small dry surface compost after Phase II, and 1- to 2-inch diameter circles, occasion- Toward the end of spawn run, perfectly spores can survive up to 18 months at ally covering up to 65 percent of the round areas may be noticed where room temperature. Severe Pythium casing, will be found. Corticium is spawn does not colonize the compost. development occurs after spores have found infrequently today because of These distinct circular areas, which may been introduced to compost at or before effective pasteurization and post-crop vary in size from a few inches up to 1–2 spawning. Airborne spores that con- steaming procedures. When this mold feet in diameter, are characteristic of taminate compost at spawning time are does appear, it may tend to persist for compost infested with Pythium. The reported to be the primary source of several consecutive crops until it is compost immediately adjacent to these infection. Therefore, filtration and concurrently eliminated from infested black areas may be well colonized with reduced spore loads during Phase II and wooden surfaces and compost. spawn and support a normal crop of spawning will help to control this mold. healthy mushrooms. Occasionally, the Apparently, spores introduced a few Overly decomposed—but not necessar- compost surface may be grown over days after spawning will not become ily wet—substrate is associated with the with spawn, but a lens or football- established in compost and will not development and occurrence of shaped mass of black compost, with the prevent spawn growth. Soil-laden straw corticium in compost. Widespread greatest diameter in the center, may be or horse manure also are thought to be infestations will result in yield reduc- found by digging into the compost. At sources of spores that survive pasteuriza- tions of up to 10 to 20 percent, and the compost’s surface, only a small (2- tion and then colonize within compost. reductions as high as 40 percent have to 3-inch) black spot may be seen, but Control also is accomplished with been reported. on digging into the compost, the sound cultural practices such as effective characteristic shape would become pasteurization of compost during Phase Corticium grows naturally as a common apparent. The compost may contain no II, a comprehensive sanitation program rotter of cellulose (dead tree limbs, signs of a pest or pathogen except for for spawning, and a complete post-crop stored straw, etc.) and profusely sporu- the sparsely growing delicate white steaming. lates when the weather is damp. It is mold, which is Pythium. Eventually, possible that spores of the Corticium- spawn may colonize the infested like fungi are carried by air currents into compost; however, few if any mush- a mushroom house before or during the rooms will grow in these areas. spawning operation, or whenever the growing room is opened to the outside environment. Improperly cured compost is a good substrate for this mold. Yield reductions can be attributed to either the mold itself, poor compost, or the combination of the two condi- tions.

66 Coprinus, or ink cap fungi, may appear Vegetatively, an ink cap fungus produces Indicator Molds during spawn run or crop production. a luxurious growth of white fine Ammonia seems to be a growth require- mycelium in or on the compost before Ink Cap Fungi ment of this fungus, and improper or after spawning. Round white pin 1 management of Phase I and II initials the sizes of peppercorns ( ⁄16-inch composting, resulting in ammonia-type diameter) begin to develop on the Common Names: compounds, is most often linked with compost sometimes as early as 3 to 4 ink caps, ink weed, wild mush- the appearance of ink cap fungi. It has days after spawning. Pins develop into rooms been suggested that variations in the mushrooms with narrow white stems Scientific Names: frequency of appearance from year to and scaly white to gray cone-shaped Coprinus fimetarius, Coprinus year may reflect the abundance of ink caps. Once the mushroom forms radiatus, Coprinus sp. caps in the straw, cobs, or hay used in (Figure 29), it disintegrates quickly into compost production, though this has ink black liquid, giving this fungi its Imperfect Stage: never been proven. Ink cap populations name, ink caps. The black liquid Ozonium, Rhacophyllus in such crops are probably influenced by characteristic of this genus is the composting and growing conditions. product of autodigestion. Certain ink cap species develop a long fibrous rhizomorph (rootlike structure) that extends into the compost.

Figure 29. After ink cap mushrooms mature, they disintegrate quickly into the ink-black liquid that gives the ink cap fungus its name.

67 Like Agaricus, the fruiting process of spawning time. The thermophilic 140°F (46 to 60°C) from 72 to 96 Coprinus is cyclical, and ink cap microflora that grow during Phase II are hours before and after pasteurization mushrooms occasionally may reappear unable to convert all the ammonia into may contain residual ammonia. Oppo- in flushes. More often though, ink cap microbial protein, and the microbes will sitely, composts that reheat (recycle) as mushrooms appear only once during use up the available carbohydrate or little as 3 to 5°F (-16 to -15°C) near the growing process. Once ammonia water before the ammonia has been the end of Phase II will have additional compounds in the compost are gone, completely converted. These ammonia- ammonia produced via microbial the compost pH decreases, and there is type compounds left in the substrate ammonification of nitrogen com- a gradual disappearance of ink caps. provide food for ink cap development. pounds. Rejuvenated microbes will use Mushroom spawn then will gradually Spotty or confined occurrences of ink previously formed protein compounds colonize the previously infested com- caps in parts of the room suggest that to obtain carbohydrates for their energy, post. these areas contain compost that is and the nitrogen left from the used packed nonuniformly or too tightly proteins may be ammonified. A low air Several species of Coprinus occur with during the filling operation. High temperature, cooler than 100°F (38°C) the mushroom crop. The larger ink cap, populations of nematodes have been and maintained to manage the internal Coprinus fimetarius, is characterized by a observed in these areas of ink caps, compost temperature, can result in an thick hollow stem and a grayish scaly further suggesting that a compacted, ammonia-laden layer (0.5 to 1 inch in cap. This mushroom often is associated tight, or wet substrate was unable to depth) at the compost surface. In such with severe substrate preparation properly heat during pasteurization and instances, ink caps can flourish on the problems, either during Phase I or Phase the remaining part of Phase II. ammonia remaining in this surface II. The smaller species, Coprinus layer. radiatus, has a shorter thinner stem and Compost moisture may favor the a very fragile pale brown to yellow development of ink caps. Overly wet Locating the origin of ink caps can aid brown cap. This mushroom often is compost is more difficult to condition, in deciding why the compost supports associated with a breakdown in supple- partially because of the reduced aeration ink cap growth. A few scattered ink caps ments added at spawning time or a within the substrate. Excessive use of are little cause for concern and may minor composting problem that steam, or steam used to maintain air indicate compost nitrogen content at resulted in ammonia-type compounds temperatures during Phase II, when too filling time near the limit for a farm. being released by the supplement. Other much fresh air is brought into the room, However, a bountiful flush of ink caps Coprinus species have been isolated from will cause condensation on the surface suggests excessive ammonia at mushroom compost, and unnamed of the compost. Excessive condensation spawnings and is evidence that certain species have been reported. will interfere with air and gas exchange aspects of Phase I or Phase II from the compost into the air during composting need to be corrected. Ink caps may begin to grow as early as Phase II. Conversely, dry compost at the end of Phase II, but more often they filling, or excessively high temperatures first appear during spawn run, after or ventilation throughout Phase II, will casing, or just before first break. result in moisture becoming the Epidemic infestation of Coprinus often limiting factor for microbial growth. is associated with a difficult or poorly Therefore, the microbes will die before managed Phase II composting. Too they are able to completely condition or much breakdown of raw materials convert ammonia into microbial during Phase I composting, which protein. The resulting ammonia-type affects resiliency or conditioning of the compounds provide a food source for compost, or the addition of too much growing ink caps. water, may contribute to a difficult Phase II and residual ammonia com- Ink caps also may grow as the result of pounds. The addition of excessive improper temperature management amounts of inorganic nitrogen to during Phase II. Areas of the compost in substrate causes an imbalance, which which the compost temperature did not also can result in residual ammonia at remain within the range of 115 to

68 Plaster Molds and Flour Molds White plaster mold first appears, near Thielavia thermophilia is thermophilic the end of Phase II or during spawn (heat loving), and for this reason is run, as a small irregular patch of white unique among indicator molds. Common Names: spawnlike aerial growth on the compost Thielavia grows rapidly and abundantly white plaster mold, brown surface (Figure 30). Within a few days, during the last days of Phase II, and is plaster mold, and flour mold this aerial hyphae begins to resemble first observed as circular- to oval-shaped Scientific Names: plaster of paris. Eventually, the aerial patches of fluffy white mold, 1 or 2 feet Scopulariopsis fimicola, growth completely disappears, leaves a in diameter, on the compost surface. Botryotrichum piluliferum, white mold on the compost surface, and Before spawning, spores in the colony Papulaspora byssina, Thielavia looks like spilled plaster or flour. In center start to mature, and the fluffy thermophila, Sporotrichum sp., some cases, the white plaster mold texture of the mold takes on a granular, Trichothecium roseum grows from the infested area of the flourlike appearance. Color changes compost and looks to be flecks of from white to salmon pink and then to Outdated Names: plaster or flour on the casing surface. beige. A few days after spawning, the Monilia fimicola, Oospoio sp., Some colonies have a pearly glisten, and white fluffy growth of this mold again Myriococcum praecox the mycelium is creamy white to buff may appear salmon pink to beige- colored instead of snow white. Other colored. The colonies may grow densely Perfect Stages: plaster or flour molds, species of and rapidly through the compost, Dichotomyces (S. fimicola), Sporotrichum and Trichothecium roseum, eventually colonizing in large areas or in Chaetomium (B. piliiliforum), appear initially as fluffy white molds many areas within the room. The Corticium (Sporotrichum), and that develop a light peach color and powdery masses of spores become Hypomyces (T. roseum) light rose-pink color, respectively. airborne when the infested area is Imperfect Stages: Acremonium, Chrysosporium, Figure 30. White plaster mold first appears as a small irregular patch of white Myceliopthora, Sepedonium, spawnlike aerial growth on the compost surface. Sporotrichum, Thielavia

Although the fungus that causes flour mold is not the same as that causing plaster mold, it is generally believed that the same nutritional factors favor the growth of the two mold groups; so they will be discussed together. Several fungi have been associated with the white and brown plaster mold condition. Briefly, Scopulariopsis fimicola probably is the most familiar, and Botryotrichum piluliferum is the most recently recog- nized. Species of Sporotrichum, Thielavia thermophila, and Trichothecium roseum have been called plaster or flour molds. Brown plaster mold has been used to describe infestations of Papulaspora byssina, Scopulariopsis fimicola, and P. byssina. The reader is referred to other references to obtain more details on the taxonomy of these fungi.

69 disturbed. Near the end of the crop to yellow or tan, and then to brown, Olive Green Mold cycle, areas infested by this mold usually orange, or rust color. Brown plaster contain numerous small black spherical mold colonies grow a bit above the Common Names: fruiting structures in addition to the compost and often are outlined by an olive green mold fluffy beige form. These fruiting bodies actively growing outer fringe of white are the sexual stage of T. thermophila. mycelium. Colonies tend not to be Scientific Names: Growth of this mold in compost occurs fluffy in structure. Several colonies can Chaetomium globosum, in conditions similar to those that favor grow together to form a continuous Chaetomium oliveaceum the growth of other brown molds and coating over the surface of the compost ink caps. It is possible that if compost or on damp bedboards. After casing, the Imperfect Stages: conditions are conducive to the growth mold may grow up through the casing Botryotrichum, Humicola, of one of these molds, several types or and emerge on the surface. The mold Papulaspora, Scopulariopsis, species may be growing in close proxim- usually is white at first, and the color Thermomyces, Trichocladium ity to each other. may change to the typical brown with a white fringe. These molds are easily The rapid growth of T. themophila in recognized by hand lens as a mass of Spores of the olive green mold fungus infested areas may increase compost darkly pigmented spherical structures are heat tolerant and may survive at temperatures to a range as high as 105 on the compost straws or casing. The 140°F (60°C) for 6 hours. However, to 120°F (41 to 49°C) and prohibit or beadlike structures, called “bulbils,” this mold appears in compost where kill spawn growth. Once the mold has appear and are interwoven with a fine Phase II ventilation is inadequate. used up its food, the compost cools, and network of white hyphae. Improperly managed Phase II aeration spawn often recolonizes the infested that leads to an inadequate oxygen level areas if ammonification of the compost It is currently thought that growth of and compost temperatures greater than has not occurred. However, these areas plaster molds and flour molds occurs 142°F (61°C) seems to promote the often fail to support either a vigorous where compost is too broken down or formation of compounds that appear spawn growth or high yields. This white overly wet during Phase I composting toxic to spawn growth but favor growth mold develops in restricted spots and and/or inadequately or improperly of olive green mold. has not been observed infesting an managed during the Phase II process. entire tray or bed of compost. Conse- These molds develop in mushroom An inconspicuous grayish-white fine quently, high compost temperatures are compost when nitrogen sources, formed mycelium growing in compost, or a fine encountered only in these spots, and during Phase I, are left after Phase II. fluffy aerial growth on the compost routine monitoring of compost tem- These nitrogen-type compounds are not surface several days after spawning are peratures during spawn run may not converted into microbial protein, are the early signs of this fungus (Figure reveal the presence of “hot spots” caused referred to as amines and amides, and 31). Spawn growth is often slowed and by T. thermophila. Presence of this most often appear in composts with pH reduced during the early part of the plaster mold is noticed most often levels above 8.5. spawn growing period. Later in spawn during a visual inspection of spawn run, this mold’s fruiting structures may growth development. It may be detected Long composting time, which results in look like very small gray-green cockle- overly composted manure, is more apt burs or peppercorns about 1⁄ inch in on farms where compost temperature is 16 monitored in a great number of to support the growth of these plaster diameter. Fruiting structures are most locations daily. Most other plaster and and flour molds. Plaster or flour molds likely to develop on straws in isolated flour molds that occur in mushroom will appear in a facility when improperly spots in the affected compost. Compost compost do not cause “hot spots.” conditioned compost is made. Although may have a musty odor and often does the spawn will grow, conditions that not support mushroom spawn growth; The brown plaster mold fungus, support widespread growth of plaster or therefore, it is common to see olive Papulaspora byssina, first appears on the flour molds will not support maximum green mold in black compost that is not compost surface during the spawn run. yields of mushrooms. Modification of colonized by mushroom spawn. The Dense plasterlike white mold may composting practices to improve fluffy white-grayish growth or green develop in areas 6 to 15 inches in compost quality usually reduces the furry burs characteristic of olive green diameter. As the fungus matures, the occurrence of flour and plaster molds. mold are obvious even on compost center of the colony changes from white colonized by mushroom spawn.

70 Characteristically, burs are olive green in of too little air sometimes is enough to Black Whisker Mold infested compost, in contrast to the cause compost to become anaerobic and blue-green spore masses of Penicillium conducive to olive green mold growth. Common Names: mold, or the forest-green Trichoderma The proportion of outside air intro- black or gray whisker mold, molds. duced into a room to ensure aerobic whisker mold conditions in the compost throughout Once it has been formed in the com- Phase II varies from facility to facility. Scientific Names: post, olive green mold persists through- Doratomyces microsporus, out a crop. Spawn usually grows into Excessive compaction or oversaturation Doratomyces stemonitis, areas occupied by Chaetomium, al- of compost with water at filling time Doratomyces purpureofuscus, though spawn growth often is delayed. should be avoided. Proper manipulation Trichusus spiralus Compost conditions conducive to a of steam valves, fresh air dampers, widespread infestation of olive green doors, and high-speed exhaust or intake Outdated Names: mold may reduce spawn growth fans can ensure the availability of Stysanus stemonitis significantly, with a coincident reduc- enough air to the compost during Phase tion in mushroom yields. II. These procedures also enhance Perfect Stages: aerobic thermogenesis in the compost, Periconia and Cephalotrichum Compost that has a good structure, such which enables compost temperatures to as that which is resilient when com- remain hotter than the air temperature pressed or not overly decomposed during Phase II. Air temperature and air Black whisker mold may occur in during Phase I, will allow for better volume should be managed to maintain compost during spawn run or after aeration during Phase II. Adequate air a temperature differential and gas casing. It first appears in spawned exchange throughout the entire Phase II exchange between the compost and the compost as an erect, black, whiskerlike is necessary to prevent compost from air. structure. The distinctive black whisker becoming anaerobic. Even a few hours appearance develops as the spores are maturing (Figure 32). Figure 31. Early signs of olive green mold are an inconspicuous grayish-white fine mycelium growing in compost, or a fine fluffy aerial growth on the compost Black whisker mold fungus in compost surface several days after spawning. indicates an unbalanced nutritional base in the compost at spawning time. When Chaetomium green mold is present, black whisker mold also will be present, since both are celluolytic, or fungi that feed on cellulose.

Black whisker mold grows rapidly through the compost at the end of Phase II and at the beginning of the spawn run. Heavily infested areas of compost appear darker than usual because of the masses of black powdery spores. When disturbed, these spores are liberated and the compost appears to be “smoking.”

Black whisker mold is not thought to be a serious competitor of mushroom spawn. Its presence usually indicates that the straw has been incompletely decomposed or caramelized. Low Phase

71 Figure 32. Black whisker mold first appears in spawned compost as erect black Smoky Mold whiskerlike structures, highly magnified in this photo. The descriptive black whisker appearance develops as the spores mature. Common Name: smoky mold

Scientific Name: (No slide) Aspergillus spp.; Penicillium spp.; Penicillium chermesinum

Several species of Penicillium have been reported in mushroom compost, and most are harmless to the spawn and overall yield; yet, it recently has been reported that P. chermesinum has caused serious crop losses when introduced into Phase II compost at spawning time. Symptoms begin to show up as edge breaks at first break. Digging into infested areas causes large clouds of spores to form; hence the name “smoky mold.” Aspergillus and Penicillium often are greenish in color, whereas P. chermesinum is characteristically white at first, then turns brown. All smell moldy.

Reported incidence of P. chermesinum occurs mostly in bulk Phase I and II systems. Other smoky molds can be found in all systems. It has been I temperatures result in excess carbohy- from these fungi, often erroneously suggested that P. chermesinum has drates that are easily used by black called “gas,” can induce an acute allergy- originated from dirty straw and from whisker mold. Black whisker mold also type response in dumping crew person- other Penicillium spp. and Aspergillus in may indicate that nitrogen supplemen- nel. Workers may report respiratory overheated, supplemented compost after tation of fresh compost ingredients was troubles often characterized by spawning. A large P. chermesinum spore inadequate, or conversely, that the asthmalike symptoms including nasal or load infecting compost at spawning has proportion of carbohydrates was too throat irritation, chest congestion, the most devastating effect on yield. high. It has been reported that this breathing difficulty, nosebleed, or Much like Trichoderma green mold, mold also grows in compost that alternating fever and chills. The there may be an interaction between the overheated during spawn run. response is transitory, but a person mycelium of this mold and Agaricus. It sensitive to these spores becomes more has been suggested that spawn is either Whether spores of black whisker mold sensitive with each exposure, and the parasitized or effectively repressed in survive peak heat is not known. Growth discomfort may become more intense. smoky mold. Control of this particular of Aspergillus and Penicillium molds also Sensitive or sensitized workers should be mold is similar to virus control; there- are favored by conditions conducive to assigned tasks elsewhere, away from fore, extreme hygiene and spore the growth of black whisker mold, and compost dumping. Proper preparation exclusion is essential. However, the these fungi also may be present in the of compost precludes the development compost. Black whisker mold, Aspergil- spores are quite small, so HEPA filters of these molds, so these molds are are required to remove these two- lus, and Penicillium are mold fungi, unknown at many facilities. which produce abundant numbers of micron spores. Cleaning before and spores. Air heavily laden with spores after spawning is essential.

72 Other smoky molds often are found in spawning, but it will not be completely Oedocephalum Mold compost where less protected spawning conditioned. These residual compounds supplements are present and overheat provide food to the bacteria or other Common Name: during spawn run or after casing. Even mesophilic (heat-loving) microbes. brown mold brief periods of temperatures above Control of these molds is ensured by 90°F (32°C) can damage or kill the compost, which is maintained in the Scientific Names: spawn. These Penicillium and Aspergillus conditioning range during Phase II until Oedocephalum sp., Oedocephalum molds easily colonize the dead spawn it is completely conditioned. It is also fimetarium grains and supplements. Compost in important that enough, but not too these areas is generally black at casing or much, moisture is in the compost. Dry sometimes has a mosaic appearance. compost may result in the microbes Brown mold may appear occasionally as Often, these black areas appear toward running out of water before they have early as during cooldown, before the center of the beds, where tempera- completely used all the available spawning, but more often develops tures are warmer (Figure 33). If the nitrogen. Conversely, wet compost during the latter part of spawn run. The overheating occurs within 2–3 days after prevents proper aeration within the mold first forms irregularly as a light spawning, residual bacteria may cause compost and prevents the microbes gray mold growing on the compost compost to begin heating. Often, from growing. surface; but within a few days, spores compost may smell clear of ammonia at form and begin to mature, and the color changes to dark tan, fawn, or light Figure 33. Compost in smoky mold-infected areas is generally black at casing, or brown. The growth habit of sometimes has a mosaic appearance. These black areas often appear toward Oedocephalum brown mold varies from the center of the beds, where temperatures are warmer. a weak growth over the compost surface to a dense coating on the compost straws. This mold grows on compost most of the time, but occasionally it is seen after casing. After casing, Oedocephalum grows slowly from sites of infestation up through the casing and may appear on the casing surface before pin formation. The pearly-white mycelium of Oedocephalum grows loosely over the surface, but its color changes to silvery brown as the fungus ages and the spores mature (Figure 34).

The appearance of this fungus, discern- ible through a hand lens, consists of an erect spore-bearing structure with a globular cluster of large spores at its top end. Rubbing Oedocephalum brown mold between the thumb and index finger produces a gritty sensation similar to that experienced in rubbing fine sand. This gritty characteristic distin- guishes Oedocephalum sp. from other white-brown molds in mushroom compost or on casing. Spores of Oedocephalum sp. are common in most mushroom composts, but they lie dormant unless induced to germinate

73 Figure 34. The pearly white Oedocephalum mycelium, discernible through a hand lens, consists of an erect spore-bearing structure with a globular cluster of large spores at its top end. Its color changes to silvery brown as the fungus ages and the spores mature.

and grow. The environmental and nutritional conditions that encourage growth are not fully understood. Usually, Oedocephalum brown mold growing in compost indicates that ammonia and amines were not com- pletely eliminated during Phase II and are serving as a food for this organism. Growth of Oedocephalum does not inhibit spawn growth, but conditions favoring its growth are not optimal for mushroom production. Compost conditions similar to those described for plaster molds are associated with the growth of Oedocephalum brown mold.

74 C. Pest Species Biology and Control

ambient temperature should be raised a Bacterial Blotch— few degrees, the humidity should be 4. Bacterial Pseudomonas tolaasii lowered to below 85 percent, and the Diseases total airflow should remain unchanged Description or increased by 10–15 percent. The goal is to lower the humidity in the growing Paul Wuest Pseudomonas tolaasii, the cause of room to induce the mushrooms to dry. bacterial blotch, is an aerobic, non- spore-forming fluorescent bacterium in Experience suggests that when the the genus Pseudomonadaceae. It is a mushroom compost is too dry when it common bacterium; many fluorescent is spawned—less than 60 percent Pseudomonads are readily isolated from H2O—the above steps will not elimi- field soil. These groups of bacteria are nate bacterial blotch from the crop. rather closely related and often difficult Also, when the source of the peat moss to distinguish, although a unique used to case the mushroom beds has feature of the species P. tolaasii is its changed, bacterial blotch may not be ability to infect and discolor commercial controlled, because some peats foster P. button mushrooms. The discoloration is tolaasii more than other peats. Another pale yellow at the start and darkens to a environmental situation in which golden yellow or rich brown color. The bacterial blotch is almost impossible to blemishes are superficial but decrease control is when the external air tem- the eye-appeal of mushrooms and lower peratures are moderate (59 to 72°F, o r their quality in the marketplace. This 15 to 22°C) both day and night, and bacterium is not a threat to human the air is full of water vapor. In such a health. situation, the condenser of the air conditioner does not turn on, since the Control air temperature in a growing room is what the grower specified. Since the Managing bacterial blotch disease on mushroom growing temperature mushrooms is a matter of chlorinating requirement has been satisfied, the the irrigation water applied to the crop moisture in the outside air is not to a concentration of 150 ppm chlorine; condensed on the cooling coils. In such using water that is potable (drinkable) instances, placing an electric light close as a source for irrigation water; and to the air temperature sensor will cause most importantly, inducing the caps of the control system to register that the the mushrooms to dry after an applica- incoming air is too warm. The con- tion of irrigation water. It is common to denser will begin to operate, which will include a 2- to 3-hour drying cycle in remove some of the excessive water from environmental management after the incoming, ambient air. irrigation. During this time, the

75 Strain Choice of the affected area getting larger as the crop aged from break to break. This There are a few reports that some wild Mummy and False symptom pattern continued until the species of Agaricus bisporus possess Mummy—Pseudomonas middle 1970s, when off-white strains resistance to bacterial blotch. In species predominated at mushroom farms, and addition, there are differing levels of Description into the 1980s, when hybrid white and susceptibility among the commercial hybrid off-white mushroom strains were strains of hybrid white and hybrid off- Mummy disease is characterized by the most widely grown strains of A. white mushrooms. Growers may be wise mushrooms that develop to the button bisporus at mushroom farms. Since then, to try different strains to determine stage or larger, then stop growing. The mummy disease seems to initially affect response to bacterial blotch, selecting affected mushrooms sometimes develop a few squares (8 to 12 lineal feet) in a the strain that performs best in the a curved stipe with translucent, longitu- growing room at traditional bed farms overall conditions at the facility. dinal streaks on the inside. The mush- and does not spread along a bed after it However, choosing a strain of A. room tissue becomes mummylike in first appears. This newer expression of bisporus based exclusively on its suscep- appearance: spongy, dry, and leathery. mummy disease, sometimes referred to tibility to bacterial blotch may not be in With an early onset of mummy disease, as false mummy, shows additional the best interests of production at a first-break mushrooms will be delayed symptoms. These include a fuzzy facility. Managing bacterial blotch is not in their development by a few days, but mycelial growth at the base of mush- simple, and sometimes the best efforts a break of mushrooms does develop and rooms (Figure 35) and very coarse fail. This approach allows a producer to can be harvested. Second-break mush- strands (rhizomorphs) attached to the choose a strain well suited for the rooms in the same location exhibit the mushrooms when picked. Also, a layer unique environmental conditions at full-blown symptoms of mummy of tissue at the base of the stipe turns each facility. disease. Thereafter, mushrooms no mahogany brown or yellow-brown longer will grow in that area. The poor when the stipe is cut longitudinally and quality of the mushrooms and the lack exposed to the air for a few minutes. of subsequent harvest from infected The bed area affected by these newer areas can create a severe economic loss. symptoms increases very little in size from break to break. If the symptomatic The causative agent that induces area is allowed to dry between breaks, mummy disease is a bacterium, a species some mushrooms will grow and can be of Pseudomonas closely related to but harvested from the affected areas. not the same as the bacterium that causes bacterial blotch. Many An unusual phenomenon has been seen Pseudomonas bacteria commonly are repeatedly when mummy disease found in and on organic matter, so it is appears in a growing room. It is doubtful the mummy bacterium is a reasonably common for the total unique organism introduced from production from the room with outside a mushroom farm. Rather, the mummy disease to be equal to or mummy bacterium may be a normal greater than the production from a part of the bacterial microflora of most room where no mummy disease occurs. mushroom composts. When conditions This oft-repeated observation suggests favor its growth and reproduction, its the bacterium associated with mummy population grows large enough to cause disease may be ecologically related to the disease recognized as mummy. one or more other organisms that are capable of enhancing production. Or, A scientist working at a cave farm in the conditions that favor mummy Missouri in the 1930s first described disease development also favor the mummy disease. It appeared as a optimum production of mushrooms. reasonably large patch of mummified mushrooms on first break, with the size

76 Figure 35. Mummy disease, showing the tilted cap and fuzzy bottom stems. Another attempt at mummy control was to water the surface of the compost with chlorinated water (150 ppm Cl) a few days before casing. Some growers were confident this practice controlled mummy; an equal or higher number assumed it enhanced the amount of mummy in a crop.

Sanitation and hygiene cannot be overlooked in efforts to control mummy disease. In their absence, mummy- infested compost moving through a tray line can contaminate the equipment, which in turn contaminates the com- post moving along behind it. One mummy-infested tray of compost can serve as an inoculum source and infest most of the other compost in one growing room of trays. At tray farms, especially, mummy disease can cause devastating crop losses. Thorough Control At farms when spawned compost is washing and sanitizing of tray-handling covered with plastic for the spawn run equipment is essential to minimize the The effectiveness of mummy control period, some growers have seen less threat of spreading the cause of mummy measures may be difficult to predict, mummy disease when they cut open disease; the same is true for spawning though moisture management is the and turn back the plastic whenever equipment. Special attention to sanita- basis for many control efforts. Experi- water accumulates on its underside. tion and good hygiene in and around ence suggests that during times of the This practice prevents the accumulated spawn bags, spawn, and the spawning year when evaporation from spawned water from dripping into the compost process is essential. compost or cased mushroom compost is and soaking the top of the bed. Sanitation and hygiene, practiced less than it should be, mummy disease In the 1970s, when off-white strains within an environment where moisture develops. Bed growers in Chester predominated, it was common practice management promotes evaporation County, Pennsylvania, have had to remove the plastic a few days before from compost and casing, are the only experiences in which the addition of casing to ensure the surface of the ways to reduce the threat of a mummy water to compost before or at the time compost was completely dry before disease infestation. of spawning predisposed the compost to casing was applied. The off-white strains supporting mummy disease. Oddly were much more sensitive than earlier though, bed growers in Berks County, strains and could be harmed by too Pennsylvania, added water to compost much water in/on the surface compost, at spawning without this response. unrelated to the mummy threat. Other factors may be involved: Berks Mummy misdiagnoses often occurred County growers generally used more when compost beds were cased when hay in blended composts, while Chester they were too wet. Under these condi- County growers use more horse manure tions, spawn growth into the casing was or straw in their blended composts. slow, mushroom formation was delayed, and the mushrooms appeared to have the characteristics of mummy disease. In fact, the problem was water stress, not mummy disease.

77 C. Pest Species Biology and Control

Introduction Nematodes 5. Nematodes Nematodes thrive in raw compost and Nematodes are tiny, very primitive Phillip S. Coles can exist in excessive numbers during roundworms. They appeared early on the mushroom growing process. While the evolutionary stage, being the first some growers believe that nematodes are animals to evolve a body cavity. They merely an indicator that compost and are extremely abundant in both types casing preparation has gone awry, it is and numbers. There are about 12,000 wiser for growers to assume that species currently known, but scientific nematodes can represent the risk of opinion holds that the number of yield losses, and to take precautions species actually could be 100 times against their proliferation. greater. Typically, nematodes range in size from 0.2 mm to 6 mm in length, though some may be much longer.

Nematodes are found in marine, freshwater, and soil habitats. It has been estimated that there are 8 billion nematodes in an average acre of field soil. One square meter of garden soil probably contains approximately 2 to 4 million nematodes. Many are parasites; in fact, almost all types of creatures studied by scientists have at least one species of nematode that parasitizes them. Roughly 50 species parasitize humans.

Caenorhabditis elegans, one of the saprophytic nematodes to be discussed below, has become an important tool for genetic and developmental research- ers. This organism is made up of only 1,000 cells. It matures in 3 days and has a transparent body that allows scientists to watch the dividing cells.

78 Compost infested with nematodes has a Nematodes in Mushroom Parasitic Nematodes characteristic appearance: soggy, sour Growing smelling, and depressed. The nematode- These nematodes, also referred to as trapping gray mold, Arthrobotrys It is fortunate that nematodes do no fungal-feeding or mycophytic nema- superba, may appear in areas where the harm in raw compost, because they are todes, are increasingly rare in mush- mycelium has been destroyed. This ubiquitous in the materials used to room farming today. Presently, industry soggy mess is apparently good habitat prepare the compost mix, and their choices of casing materials or pasteuriza- for the saprophytic nematodes, the complete removal, if possible, would be tion of casing usually avoid outbreaks. second of the two types discussed here, extraordinarily expensive. The richness In the past, however, they were respon- for they frequently appear in these areas. of the compost environment in terms of sible for disastrous crop losses. food, water, and oxygen provides nematodes with an excellent habitat, at The parasitic nematodes use their stylet least until composting temperatures (a needlelike mouthpart) to pierce the reach lethal ranges. The cooler outer mycelial cell and inject digestive juices. portions of the rick, if not mixed and The same stylet then becomes straw turned into the interior, will continue to through which the nematode consumes support nematode populations into the liquefied cell contents. As nema- Phase II. todes move through the mycelium-filled compost, they first destroy the fine There are four general types of nema- hyphal structures and leave the myce- todes: parasitic, saprophytic, predatory, lium looking stringy. Thereafter, larger and animal parasitic. Only the first two mycelium is destroyed, leaving small are discussed here. For mushroom barren bed areas that grow progressively growers, the primary difference between larger as the nematodes venture outward these two groups lies in their feeding into healthy compost. If the conditions habits. The parasitic nematode feeds are optimal for the nematodes— directly on mushroom mycelium, moderate temperature (68–77°F, 20– whereas the saprophytic nematode feeds 25°C) and wetness—entire beds can be on bacteria, protozoa, fungal spores, and denuded of their mycelium. Depending other bits of organic matter, but does on the number of nematodes on the not attack the mycelium. bed, the mushroom crop will be reduced or eliminated.

Under good conditions, nematodes can multiply 30- to 100-fold in 2 weeks. When their burgeoning population exhausts the compost of its nutrients, the nematodes respond to the changing environment by swarming to the surface. Exposed there, they can be picked up easily by vectors such as humans and flies. If dried slowly, the nematodes become dormant and can be distributed by even slight air move- ments.

79 At low levels, these nematodes have Effects on mushrooms can range from Saprophytic Nematodes little effect on mycelium. As the little damage to total elimination of the nematode numbers increase, mycelium crop. The appearance of the compost These nematodes, often referred to as begins to grow slowly and weakly. At can gives clues to the damage to come; “free-living,” now are more commonly high infestation levels, the strands when dark, watery, barren patches associated with mushroom farming than completely degenerate. Research develop, production will be severely the parasitic species. They characterize suggests that the extent of the affected. poorly prepared compost and/or casing saprophytic nematode damage to and cause severe deterioration of mycelium is closely tied to the number mycelium in their own right. The of bacteria, the nematodes’ primary Survival Characteristics common saprophytic species are listed food source, present in the spawned below. In most cases of infestation, two compost or casing. Their detrimental Nematodes owe their abundance and species of these nematodes are present. effects on the mycelium appear to be linked to the release of a toxin or widespread distribution in part to their byproduct into the compost. Extracts remarkable survival abilities. If dried taken from diseased compost and casing slowly, they enter a heat-resistant Common Saprophytic Nematode dormant state that can persist for years Species show there is greater crop damage when both bacteria and nematodes are present until they contact enough moisture to Acrobeloides apliticus in high numbers than when only break dormancy. In the dried state, they are distributed easily by air currents. Acrobeloides buetschii bacteria are present. The enhanced crop injury may be the result of increased They also can survive without food for Caenorhabditis elegans production of toxins when both are months. They are not susceptible to Cruzenema lambdiensis present, or may reflect some way in cold or freezing, and they regain their which the nematodes make possible a vigor once temperatures are more Panagrolalmus rigidus more rapid or thorough bacterial moderate. When their high numbers Pelodera (Pelodera) strongyloides colonization of the compost. begin to deplete the readily available food supplies in compost, they show a Rhabditis (Cephaloboides) oxycera There is an interesting ecological collective swarming behavior that brings Rhabditis (Choriorhabditis) relationship among the nematodes, them to the compost surface for a longicaudatus bacteria, and mycelium. Under exces- greater chance of dispersal. The Rhabditis (Rhabditis) terricola sively wet compost conditions, bacteria saprophytic nematodes take this group have an advantage over mycelium, and behavior a step further and form into Rhabditis (Pellioditis) pellio as the nematode food source, their columns of living nematodes, hundreds increase in numbers encourages the strong, that wave about on the surface expansion of the nematode population. of the mushroom bed, ready to adhere Saprophytic nematodes’ feeding habits The high numbers of bacteria also to hands, tools, flies, or other objects. differ markedly from their parasitic inhibit normal growth of mycelium. This phenomenon is called winking. counterparts. They suck in and chew The compost deteriorates and becomes The waving strands of winking nema- the particles of food they consume. wet and increasingly anaerobic. Under todes can be observed by holding a They possess a muscular pharyngeal less wet conditions, the mycelium can flashlight at a 45-degree angle to the bulb, which creates the suction to draw spread, use the water for its own bed. A grower’s IPM plan should take in food particles and liquids. The growth, and dry out the compost to a into account these survival traits to saprophytic nematodes multiply even point that inhibits the bacterial prolif- minimize the opportunities for nema- faster—one hundred-fold in 3 days— eration. The nematodes remain in low tode dispersal. than those that are parasitic. Many of number because of the dry conditions these nematodes are parthenogenetic and the limited food source. The (self-fertile). environment remains favorable for mushroom production.

80 Another source of nematodes in a crop Sources of Inoculum is a preceding infested crop. In growing Sampling, Separation, and rooms, woodwork and ceiling insulation Identification Nematodes are carried into the growing contaminated with nematodes can process in a number of ways; the most inoculate successive crops. If high Ricks, trays, or beds that are suspected obvious of which is in the compost. As temperatures during pasteurization do of infestation can be tested for presence noted above, nematodes are associated not penetrate into the wood, especially and relative quantity of nematodes. In with raw materials entering the compost into the cracks and crevices, nematodes any testing procedure, the integrity of yard and respond by proliferating in the will not be destroyed. Likewise, mois- the sample is critical; in this case, the initially favorable compost environ- ture dripping from contaminated ceiling location at which the sample is collected ment. On the cooler parts of the rick, insulation spreads nematodes to new can strongly influence the results. inside clumps of compost materials, or beds. Collecting samples from the hottest in excessively wet compost, they may portions of the materials usually will Nematodes can invade growing rooms survive Phase I and enter Phase II. The give negative results because nematodes from other areas of production in a vast majority of their population may be rarely survive there. Sampling at cool variety of ways. Dust can carry dormant destroyed in a Phase II room during locations or areas where heating has nematodes between rooms, and flies, pasteurization at about 140°F (60°C), been nonuniform in the past is more mites, hands, boots, and tools can carry but survivors can persist in wet areas, likely to produce detection of the pests. nematodes acquired from contact with dry areas, and clumps, and can continue Incubation of samples sometimes is swarms or contaminated materials. on to spawning. There they encounter a necessary to provide adult nematodes Equipment such as spawning machines, more favorable environment: tempera- for identification. if not designed for easy cleaning and if tures around 75°F (24°C), moist not routinely sanitized, provide nema- conditions, and near-neutral pH (7.5). Nematodes can be separated from todes with an effective means of Mixing at spawning distributes the compost or casing and identified distribution. nematodes. The spawning machine can visually. A Baermann funnel (Figure 36) contaminate many subsequent beds or is a convenient tool for collecting trays after spawning a single infested nematodes for further investigation. The batch of Phase II compost. apparatus consists of a support system that holds a funnel with a bottom tap Peat, as it is introduced into the closure. The funnel is filled with fresh growing process, is dry, has a low pH, water. A cloth or strong, fine mesh bag and usually does not contain nema- is suspended over the water at the top of todes. Once in place as casing, however, the funnel. Strong commercial tissues as conditions become more moist, peat will work. A sample of compost or provides a favorable environment. casing is placed into the bag. The Compared to compost, casing provides nematodes move out of the sample, and a habitat with less interference by since they are slightly denser than water, mycelium. Pasteurization temperatures, sink down the funnel until they are as noted above, and careful watering stopped by the tap closure. The tap (moist but not wet) can reduce or closure is opened after the migration has eliminate nematode populations; but proceeded for several hours, and the failure to manage these environmental nematodes are collected in a shallow conditions can allow nematodes to glass dish. move further into the growing process. Nematode identification by nonexperts is limited to differentiation of general type or genus level. The most useful distinguishing characteristic is the appearance of the anterior (front) end where the mouthparts are located. A

81 Figure 36. A Baermann funnel is a simple tool for extracting nematodes from material. Control Measures

Because nematodes are ubiquitous, total prevention of nematode invasion and total eradication during infestations is unlikely. Further, since nematicides are not available to mushroom growers, measures to prevent or control infesta- tions are limited to ensuring that normal temperature and sanitation safeguards are followed, and that enhanced measures are instituted when necessary. A well-prepared IPM pro- gram should outline clearly these measures and help keep all members of the growing team on track.

The Phase I rick provides the grower with his first opportunity for nematode control. Good Phase I temperatures, uniform mixing of the raw materials, and ensuring that cool shoulders are moved to the interior positions are measures that will reduce the number of nematodes moving on to Phase II.

Compost should be pasteurized at 140°F (60°C) for 2 hours to subject the nematodes to killing temperatures. This temperature range is adequate to kill wet nematodes, but if the compost and nematodes dry out, temperatures as high as 160°F (71°C) would be required for lethal effect. The compost may require moisture adjustment to avoid being overly dry, but care should be taken not to make the compost soggy, blunt end from which the needle-like mined well enough to make control or bacterial development will be stylet can extend shows the organism to judgments or to process comparisons. encouraged. The heating system should be parasitic. Saprophytic nematodes But, for the grower, simply the existence be checked and compost temperatures lack the stylet and appear to have liplike of nematodes, regardless of the species, monitored to verify that uniform peak bulbs stuck on their anterior ends. By is a problem. heats are reached in all areas of the noting the structures of the anterior compost. Casing should be pasteurized end, the shape and size of the internal at 140°F (60°C) unless the grower is structures, the body length and other confident that each shipment is free of features, and contrasting them to nematodes. Recontamination of the published illustrations of nematode casing should be avoided. types (rhabditoid, aphelenchoid, etc.), the nematodes’ identity can be deter-

82 At spawning, any compost suspected of These control measures should be farm operation or even the season of the harboring significant nematode popula- used as the basis of a grower’s control year. The two case histories below tions should be processed last and program, but in certain cases, illustrate creative problem solving in followed by scrupulous cleanup of infestations appear that require nematode control. machinery. During cropping, the remedies tailored to the particular grower can do little to control an infestation other that to prevent further spread. One of a grower’s challenges is to rid the growing room of its legacy of Case History #1: Ross and Burden nematodes. Pasteurization at tempera- tures of 160°F (71°C) should be (as presented in “An unusual problem—saprophagous nematodes.” Mushroom conducted. News. January 1982.) Scrupulous attention to sanitation throughout the growing process, the Ross and Burden describe sudden, massive crop losses that were traced hallmark of a properly maintained farm, eventually to saprophytic nematode (Rhabditis) infestations. In the first occur- will contribute greatly to nematode rence, the farm’s production dropped 50% in two weeks, and in a later instance, control. In addition to typical sanitation practices, the following should be dropped to 10% of budgeted levels. Ross and Burden observed lost production considered: in the first break, with barren patches appearing on some trays. Other trays were

● Develop and enforce rules restrict- completely barren. Mycelial degeneration was evident, pinning was poor, and ing personnel movement between large numbers of nematodes became visible. compost areas and growing rooms. Their investigations uncovered, among other things, that the production problem ● If trays, shelf boards, or other such items cannot be pasteurized, they was worse on trays that were watered at spawning, and that significant numbers can be washed with a steam of nematodes were surviving peak heat. After further investigation, they con- pressure washer—though this cluded that active compost (which also had a higher-than-normal initial load of treatment may be insufficient to nematodes) required extra fresh air in Phase II. However, the air/bed temperature kill all nematodes. Sanitizers should be used in rooms and on equip- differential was sufficient to dry and cool the surface of the compost, a condition ment. This is especially important that protected the nematodes from heat kill. Flooding during the same period on floors, since they act as a heat likely had carried many nematodes into the farm, providing the unusually high sink during pasteurization and rarely can have their temperatures pest pressure. The coincidence of the extra burden of pests and the surface raised sufficiently to kill nema- drying in Phase II set off the chain of events that resulted in catastrophic infesta- todes. tion. They reported, “A few simple anti-nematode measures were put into

● Redouble sanitation efforts at operation, and the farm yield recovered very quickly. . . .” spawning. Review spawning machine design and positioning to This incident and another nematode problem with a shelf operation provided the determine if better cleaning is investigators’ impetus to delve further into the factors influencing nematode possible with adjustments or infestation. They concluded that saprophytic nematodes could be a primary retrofitting. cause of crop losses. ● Take precautions against nematode spread by bits of spilled compost from infested trays. Clean up any dropped materials before they are carried into noninfested areas.

83 strains are not available yet, but their pursuit is a worthwhile venture for Case History #2: Barber and Cantarera researchers.

(as presented in “Seasonal nematode problems.” Mushroom News. June 1987.) Conclusion Barber and Cantarera described a common phenomenon, occurring in late

winter and spring in southeastern Pennsylvania, of dramatic increases in This section could not end with a better nematode populations in crops ready to pin. They suggested a cause and message than that contained in the last described measures to remedy the problem. sentence of Case History #2. A compla- cent opinion that will not serve the The phenomenon, they wrote, has its origin in the cold shoulders found in grower well is that nematodes, especially saprophytic nematodes, are not really compost ricks during the winter months. If effective cross-mixing of the rick is pests, or that they are only indicators of not accomplished, these regions fail to achieve the temperatures necessary for other problems. A valid IPM program nematode kill. This extra load of nematodes is carried into Phase II, where routine must consider the potential for nema- tode infestation and detail all farm- pasteurization practices may be unable to bring nematode populations down to specific anti-nematode measures to safe levels. Barber and Cantarera suggest that sampling of Phase II trays in avoid expensive crop loss, especially locations likely to be cooler (near sideboards, ends, and surfaces) gives a better since pesticides are not an option. indication of nematode survival than sampling the centers of trays. When swarming of nematodes is observed before pinning or by first break, the grower can safely assume that Phase II pasteurization has fallen short of expectations. Dryness may be the cause, and moistening the compost surface at fill or just before pasteurization assists the normal peak heats in producing the necessary kill. However, the wetting must be judicious and soaking avoided. These simple measures have mitigated seasonal nematode problems. They warn farmers to avoid the belief that nematodes are “not really harmful.”

carrying spores through the compost or casing. Research has shown that The Future Arthrobotrys irregularis kills nematodes, but use of this fungus has not developed The future may hold new options for a wide following. nematode control. At the present, we have few ways of dealing with nema- A great aid to the grower would be the todes once they are infesting a bed. But development of strains resistant to the new applications of biological control toxins that are suspected of being may change that. Nematode-trapping produced in nematode infestations. Off- fungi, for example, hold promise for white and white strains were shown pest control. These fungi can pierce the years ago to react differently to extracts outer surface (cuticle) of nematodes, prepared from nematode-infested invade their bodies, and lay spores on compost and casing, giving rise to hopes the inside. In the process, the nematode for commercially effective levels of is killed, but before death comes, its resistance in the hybrid mushroom movements can disperse the fungi by strains used today. Unfortunately, such

84 C. Pest Species Biology and Control

Introduction History of Virus Disease 6. Virus Disease Of all the diseases confronting the Virus disease, which also is known as La C. Peter Romaine grower, none has been the subject of France disease, dieback, X disease, more confusion than virus disease. It watery stipe, and brown disease, was has been known by a variety of names, noted first in 1948 by James Sinden and shows a wide range of symptoms, and in Edith Hauser on the La France Brothers the early stages, can be overlooked mushroom farm located in southeastern completely. Virus disease can be Pennsylvania. The disease was reported confused with the effect of poor cultural later in England and the Netherlands, practice. It is increasingly apparent, and probably occurs worldwide. though, that the economic impact of We now are confident that La France virus disease is significant and realized disease is caused by a virus. During the worldwide. 1960s, Michael Hollings in England proposed that a virus caused this disease. He prepared extracts from diseased mushrooms and found that they contained several types of viruslike particles when viewed at a high magnifi- cation with an electron microscope.

The scientific confirmation of the viral cause of the disease did not come easily or quickly. Only after many years of scientific research was the identity of these viruslike particles determined with some certainty. It is now known that there are at least three types of viruses of interest to mushroom growers. La France isometric virus (LIV) is thought to be the main cause of virus disease. Mushroom bacilliform virus (MBV) is associated with the disease, but may be a benign virus. Vesicle virus (VV) also appears to be a benign virus that is widely distributed in commercial mushrooms.

85 Figure 37. Symptoms of virus disease. Shown is the characteristic “drumstick” syndrome involving elongated stems and small, misshapen caps.

elevated level of CO2. The mushrooms noticed at all, it may be confused with Disease Symptoms are poorly anchored in the casing, and the effect of suboptimal cultural their veils open prematurely and conditions. It is critical that the grower Part of the confusion surrounding virus discharge spores. Nematodes and arranges for clinical testing of the crop disease likely resulted from the range of lipstick mold may be abundant in the for the presence of virus, to confirm the symptoms by which the disease presents compost, indicating inadequate and existence of the disease once it is itself. The disease can reveal itself in two nonuniform peak heats in Phase I and suspected. severity ranges. In its less severe form, Phase II. In many cases of severe virus Observations over the years have given the virus causes only minor yield losses. disease, the casing shows spots com- clues to the factors influencing the Mushrooms have a normal appearance, pletely barren of mycelium; these areas severity of the disease: although yield may be slightly de- fail to develop mushrooms. This pressed, and the crop appears to be “dieback” syndrome probably is related ● Generally, the greater the square suffering the effect of poor cultural to high populations of nematodes rather footage of a bed showing disease practices. than to the direct effects of viral symptoms and the earlier the infection. symptoms appear, the greater the In the more severe form, the disease crop loss. causes a delay in the emergence of While the severe form of virus disease is mushrooms. When the mushrooms dramatic, much of the economic impact ● The closer infection occurs to the appear, they have small caps and long is caused by the yield loss associated time of spawning, the more severe stems that growers refer to as the with the less severe form. This yield the disease. Contaminated compost “drumstick syndrome” (Figure 37). The depression can occur early on, before produces a severe infection if mixed mushrooms may look similar to those the grower suspects virus disease has into noncontaminated compost at grown in an atmosphere with an effected a crop. If the slight yield loss is spawning.

86 ● The earlier in the cropping cycle LIV is the infectious agent that has been infection occurs, the greater the The Viruses implicated in virus disease. LIV is found crop loss, since most mushrooms in all virus disease-affected mushrooms. appear in the early breaks. A trained researcher can detect many MBV is not considered a cause of virus kinds of viruses “lurking” in mush- disease. Research has shown that MBV ● All mushroom varieties are suscep- rooms, but very few viruses have any is present in some healthy mushrooms, tible to virus disease. There is known impact on the appearance or but it also is present in most, but not anecdotal evidence that brown growth of the mushroom. The same is all, mushrooms affected by virus strains are more resistant than off- true in all the organisms that scientists disease—but never without LIV being white and white hybrid strains, have studied. We also harbor many present too. LIV seems quite capable of although the purported degree of viruses in our bodies that seem to have causing disease without the assistance of resistance has never been quantified. no discernible effect on us at all, and we MBV. It is suspicious, however, that In the absence of resistant strains, are concerned only about those that both MBV and LIV are detected in control of the disease remains in the cause disease. most cases of virus disease. MBV hands of the grower. conceivably could modify the severity of The mushroom viruses that have been the disease symptoms or may cause studied so far are composed of the another type of disease not yet de- genetic information-encoding chemical scribed. Or, it may have no effect on the ribonucleic acid (RNA). A protective mushroom whatsoever. VV occurs in protein coat covers the RNA, but in the both healthy mushrooms and those case of the VV, a lipid membrane showing virus disease symptoms, and replaces the protein shell. for this reason is thought to be benign.

Viruses multiply to astronomical The table below summarizes our current numbers within the cells of their host, understanding of the occurrence of but they lack the biochemical features to these three viruses in healthy mush- do so on their own. Consequently, they rooms and in mushrooms showing must reproduce inside a host cell; in symptoms of virus disease. effect, they take over the operations of the cell for their own multiplication. For this reason, viruses are considered nonliving “molecular pirates.” For the same reason, mushroom viruses are not transmitted as “free-living” particles within the compost, casing, or water, but rather are transmitted only from within a living organism (i.e., mush- room spores and mycelium).

Incidence of the Virus in:

Virus Type Healthy Mushrooms Diseased Mushrooms

LIV <1% 100%

MBV ~5% ~60%, but only with LIV

VV 100% 100%

87 Spore-transmitted virus disease tends to Sources of Infection be less severe than mycelium-transmit- Patterns of Infection ted virus disease, possibly because of the LIV associated with virus disease is extra time necessary for spores to Now that virus disease is recognized in transmitted through spores and myce- germinate before infecting mycelium its various forms, growers have been lium of the mushroom. Transmission of and spreading throughout a crop of able to discern certain patterns of the virus by infected mushroom mushrooms. This delay is somewhat infection. Historically, the disease mycelium in the compost was investi- offset by the large number of spores commonly flared up when construction gated even before the viral nature of the available to carry the virus. on the farm disturbed a settlement of disease was known. It was shown that virus-infected spores. Typically, growers infected mycelium could, if introduced observed the disease in crops that were experimentally or accidentally on being spawned at or near the time of the untreated wooden surfaces, carry the construction. More recently, outbreaks virus into a healthy crop. The healthy have been associated with a composting crop then would develop the symptoms problem. Much like an indicator mold, of the disease. Virus transmission by virus disease shows that the compost is way of infected mycelium has been not being heated uniformly to tempera- associated with severe disease outbreaks, tures that are high enough to destroy possibly owing to the ability of the the sources of the virus in the compost. mycelium to fuse quickly with the healthy spawn and transmit the virus.

Spores now are believed to be the most important mechanism for spread of the virus. Spores are produced in prodigious numbers within mushroom farms. One mushroom can discharge 1.3 billion spores, and spore discharge rates from exhaust air can be as high as 3.7 billion per minute. Though diseased mush- rooms produce fewer spores than healthy ones, almost 70 percent of the viable spores discharged by diseased mushrooms contain LIV. When a diseased spore germinates in compost, it sends out its own mycelium, which can infect healthy mycelium (i.e., spawn). As rhizomorphs and mushrooms develop from the infected mycelium, the virus multiplies and spreads throughout the tissues, causing disease and infecting the new mushrooms and their spores. Picking mushrooms tight stops this disease-spreading cycle by preventing the release of spores. Since diseased mushrooms tend to open and release their spores prematurely com- pared to healthy mushrooms, growers must be very diligent in their picking practices.

88 Figure 38. Clinical diagnosis of virus disease. DsRNA analysis (left) and RT-PCR analysis (right) of healthy (Hea) and diseased (Dis) mushrooms. DsRNA analysis Clinical Diagnosis of Virus detects a vesicle virus dsRNA in healthy mushrooms, and numerous La France Disease isometric virus dsRNAs in diseased mushrooms. RT-PCR detects only La France isometric virus in diseased mushrooms with the presence of a specific DNA product (arrow). DNA size markers are shown (Mkr). Clinical diagnosis of virus disease can be a critical part of an IPM program. As noted earlier, clinical diagnosis of viruses in a crop is an important first step in correcting an outbreak, espe- cially when the disease is manifesting its milder form. Testing for virus disease is useful in other ways. The grower should routinely test to determine if virus disease is present but unnoticed in crops. This precaution can pay for itself in reduced yield loss. Once a virus outbreak occurs, the grower can use virus testing to monitor the course of the infection to verify that control measures are successful. How this testing is performed has changed and improved in recent years. Testing is now extremely sensitive, available, and Reverse-transcription polymerase chain affordable. Some commercial spawn reaction (RT-PCR) is the state-of-the- manufacturers offer virus diagnosis as a Control Measures science test that now offers unsurpassed customer service. sensitivity for virus disease diagnosis. In Since there is no known commercial this test, an enzyme to DNA first Early on, viruses were detected visually mushroom strain that is resistant to converts the viral dsRNA. Using using an electron microscope alone or in virus disease, the grower must incorpo- another enzyme, the DNA then is combination with antibodies rate virus disease preventative measures copied more than a million times, (immunosorbent electron microscopy) into the IPM plan and rigorously carry similar to using a photocopier. The large that captured the virus particles, making out the control measures. The following quantity of the copied DNA can be them easier to detect. This testing practices are recommended for disease detected easily in the laboratory, even procedure is expensive, but it is still control: used in parts of Europe. though the original viral RNA from which it was copied may have been ● Establish and strictly adhere to a Testing for the presence of certain present in the mushroom tissue at levels complete sanitation/hygiene double-stranded RNAs (dsRNAs), the too low to detect by other methods program. Sanitation of surfaces, genetic component of the virus, was (Figure 38). Using RT-PCR, virus machinery, and clothing of workers widely practiced in the 1980s and was testing can be extremely sensitive, and is the foundation of the control the research tool that led to the identifi- few virus episodes escape undetected. program. Disinfectants (quaternary cation of LIV as the virus disease agent The test is of reasonable cost and does ammonia solutions, iodine, phenolics, (Figure 38). This test was used at farms not require extraordinarily expensive lab and chlorine) can be used in the to diagnose, detect, and monitor virus equipment. cleaning regimes. outbreaks. Its use allowed growers to track progress through the course of ● Control the release and movement outbreaks, match results with control of spores to prevent them from practices, and verify when virus out- infecting new crops. Do not allow breaks actually had disappeared. mushrooms on the beds to open; pick tight. Pick diseased crops last.

89 Use HEPA air filters on production room air intakes. The Future

● Attend to composting and pasteur- Considerable success has been achieved ization. Adequate and uniform in genetically engineering viral resis- peak heats are necessary to kill tance in plants, and work is under way sources of infection in the compost to accomplish the same for mushrooms. (virus-infected spores and mycel- The first highly efficient and convenient ium). Check routinely to ensure procedure for transferring genes into pasteurization with good peak Agaricus bisporus recently was developed heating during Phase II. (C. P. Romaine laboratory). Through molecular biotechnology, the breeding ● Be careful to avoid contamination of viral-resistant mushroom strains, as during spawning operations, and well as strains with wide-ranging novel be protective of spawned beds. traits, now is within our grasp. Practice thorough sanitation during spawning operations. Movement of workers should be restricted in the area where spawning operations are carried out and where spawn run crops are growing. Use plastic sheets on beds during spawn run to prevent spores from falling on the compost.

● Time-released supplementation at spawning may improve yields from a diseased crop, but is not a substitute for any of the control measures listed here. It cannot control the disease.

● Steam off to kill sources of infection such as mushroom spores and mycelium. Usually 160°F (71°C) in the beds for 6 hours or more is effective. Some growers use a 24- to 48-hour steam-off. Double steaming the house, once when full and again when empty, has been practiced but probably is not any more effective than steaming the house properly once.

90 Contributors Visit Penn State’s College of Agricultural Sciences on the Web: http://www.cas.psu.edu

Phillip S. Coles, project coordinator and Penn State College of Agricultural Sciences research, contributor, project manager, Giorgi extension, and resident education programs are funded in part by Pennsylvania counties, the Mushroom Company, and chair, Commonwealth of Pennsylvania, and the U.S. Integrated Pest Management Commit- Department of Agriculture. tee, American Mushroom Institute This publication is available from the Publications Distribution Center, The Pennsylvania State William Barber, growing manager, University, 112 Agricultural Administration Giorgi Mushroom Company Building, University Park, PA 16802. For informa- tion telephone (814) 865-6713.

David M. Beyer, assistant professor of Where trade names appear, no discrimination is plant pathology, The Pennsylvania State intended, and no endorsement by the Penn State College of Agricultural Sciences is implied. University Issued in furtherance of Cooperative Extension Shelby J. Fleischer, associate professor of Work, Acts of Congress May 8 and June 30, 1914, entomology, The Pennsylvania State in cooperation with the U.S. Department of Agriculture and the Pennsylvania Legislature. T. R. University Alter, Director of Cooperative Extension, The Pennsylvania State University. Cliff Keil, associate professor of ento- This publication is available in alternative mology and applied ecology, University media on request. of Delaware The Pennsylvania State University is committed to Danny Lee Rinker, associate professor, the policy that all persons shall have equal access to programs, facilities, admission, and employment mushroom specialist, Horticultural without regard to personal characteristics not related Research Institute of Ontario to ability, performance, or qualifications as determined by University policy or by state or C. Peter Romaine, professor of plant federal authorities. It is the policy of the University to maintain an academic and work environment free pathology, The Pennsylvania State of discrimination, including harassment. The University Pennsylvania State University prohibits discrimina- tion and harassment against any person because of age, ancestry, color, disability or handicap, national Susan P. Whitney, extension specialist in origin, race, religious creed, sex, sexual orientation, entomology and applied ecology, or veteran status. Discrimination or harassment University of Delaware against faculty, staff, or students will not be tolerated at The Pennsylvania State University. Direct all inquiries regarding the nondiscrimination policy to Paul Wuest, professor emeritus of plant the Affirmative Action Director, The Pennsylvania pathology, The Pennsylvania State State University, 201 Willard Building, University University Park, PA 16802-2801, Tel 814-865-4700/V, 814- 863-1150/TTY.

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