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Phytoprotection

Use of Fungi for Pest Control in Sustainable Agriculture Siegfried Keller

OECD Workshop - Sustainable Pest Management, Safe Utilization of Résumé de l'article New Organisms in Biological Control. Montréal, Québec, Canada. The registration procedures for microbial pesticides have been based by and September 27-30, 1998. large on those developed for registration of chemical pesticides. However, Atelier de l’OCDE - Gestion durable des ennemis des cultures, fungi as living organisms differ in many aspects from inert substances. These Utilisation sécuritaire de nouveaux organismes de lutte biologique. differences are pointed out and discussed in the light of practical experiences. Montréal, Québec, Canada. 27-30 Septembre 1998. A pragmatic registration procedure is proposed taking into account the use of a Volume 79, numéro 4, 1998 based product in relation to its natural distribution and behaviour. On the one hand, the use of a fungus naturally occurring on the target host does not need a sophisticated registration procedure. On the other hand, however, a URI : https://id.erudit.org/iderudit/706158ar genetically altered fungus applied against a non natural host in a non natural DOI : https://doi.org/10.7202/706158ar habitat needs very careful examination.

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Éditeur(s) Société de protection des plantes du Québec (SPPQ)l

ISSN 0031-9511 (imprimé) 1710-1603 (numérique)

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Citer cet article Keller, S. (1998). Use of Fungi for Pest Control in Sustainable Agriculture. Phytoprotection, 79(4), 56–60. https://doi.org/10.7202/706158ar

La société de protection des plantes du Québec, 1998 Ce document est protégé par la loi sur le droit d’auteur. L’utilisation des services d’Érudit (y compris la reproduction) est assujettie à sa politique d’utilisation que vous pouvez consulter en ligne. https://apropos.erudit.org/fr/usagers/politique-dutilisation/

Cet article est diffusé et préservé par Érudit. Érudit est un consortium interuniversitaire sans but lucratif composé de l’Université de Montréal, l’Université Laval et l’Université du Québec à Montréal. Il a pour mission la promotion et la valorisation de la recherche. https://www.erudit.org/fr/ Research Challenges and Needs for Safe Use of Microbial Organisms

Use of Fungi for Pest Control in Sustainable Agriculture

Siegfried Keller

Swiss Fédéral Research Station for Agroecology and Agriculture, Reckenholz, CH-8046 Zurich

ABSTRACT animais. This diversity bears an enor- mous potential for pest and vector con­ trol. In the future, therefore, and espe- The registration procédures for micro­ cially in the context of the efforts to bial pesticides hâve been based by and favour sustainable agriculture, we can large on those developed for registra­ expect a considérable increase in the tion of chemical pesticides. However, use of fungi for pest control. fungi as living organisms differ in many aspects from inert substances. Thèse The preferred environment for Hy­ différences are pointed out and dis- phomycetes and Cordyceps is the soil cussed in the light of practical expéri­ whereas nearly ail Entomophthorales ences. A pragmatic registration procé­ are found above the soil level. Most dure is proposed taking into account species are spécifie pathogens and at­ the use of a fungus based product in tack single host species or a limited relation to its natural distribution and number of related host species. The behaviour. On the one hand, the use of entomopathogenic soil fungi are char- a fungus naturally occurring on the acterised by small conidia, relatively low target host does not need a sophisticat- virulence (i.e. a large number of conidia ed registration procédure. On the other is needed to infect and kill the host), a hand, however, a genetically altered relatively long incubation time and a fungus applied against a non natural slow self propagation. In contrast, the host in a non natural habitat needs very Entomophthorales hâve large structures careful examination. and resting spores, a single conidium or few conidia can infect and kill the host, death occurs within a few days INTRODUCTION and the self propagation is fast. Thèse characteristics must be considered as Several hundred species of fungi are an adaptation to the environment and known to infect and kill and hâve implications for their use as mi­ mites. The most important groups are crobial control agents. the within gênera like , , Verticillium, and , the Asco- USE OF FUNGI mycetes within the Cordyceps FOR PEST CONTROL and the Entomophthorales with a total of 12 gênera and some 230 and Fungi are important enemies of many mite pathogenic species. The latter is pest species and are able to control nearly unexploited although 30% of pest populations naturally. There are thèse attack pest species or vectors of twofundamentally différent waysto use diseases of humans and domestic fungi for pest control:

56 1. Favouring those being présent natu- mycélium, hyphal bodies or resting rally by manipulation of the environ- stages. ment (e.g. habitat management). This Under favourable conditions the fun­ will not be discussed hère although gus switches to the saprophytic phase. it is an important strategy for sus- Hyphae or conidiophores émerge from tainable agriculture. their host by penetrating the host cuti- 2. In vitro or in vivo production and cle from within the cadaver. The Ento- application. The fungus can be intro- mophthorales form a single layer of duced into the host population with conidia on the host surface, whereas a single application using technical the Hyphomycetes form a more or less equipment or autodissemination conspicuous mycelial mat around the techniques, or it can be applied re- host which produces the conidia, the peatedly like a chemical. The aim of structures responsible for dissémina­ the application is to achieve short- tion and infection of new hosts. term or long-term control, to enhance epizootics and/or to establish the Factors related to the organismic pathogen in the host population. character Genetic diversity: Any fungal species There are several examples in the possesses a genetic diversity which can literature demonstrating the successful be used to subdivide it into strains. use of thèse techniques for pest control Thèse strains can show différent reac­ like the introduction and release of tions to abiotic factors such as environ- Entomophaga maimaiga resulting in mental conditions, nutrients or Chemi­ epizootics and long-term control of the cals including pesticides, or to biotic gypsy moth in north-eastern USA, the factors such as virulence or persistence. treatmentof adultcockchaferwith Beau- veria brongniartii using the females as Host range/specificity: Under natural vectors of the disease to contaminate conditions most species hâve a limited the breeding sites resulting in long-term host range. But species with a wide host control in north-eastern Switzerland or range also tend to be more virulent for the repeated treatment of spittle-bugs the host from which they were original- with Metarhizium anisopliae in Brazil. ly isolated. They can be classified into Other techniques applied to ento- pathotypes based on their specificity. mopathogenic fungi like transgenic or Self-propagation: A limited number of genetically altered strains or their use fungal spores are able to start a multi­ as endophytes are not discussed hère. plication process, which results in a thousand to billion fold increase of the spore amount. This can also happen at FUNGI ARE DIFFERENT the population level as a resuit of an FROM CHEMICALS outbreak or the induction of an epizoot- ic which can resuit in remarkable aerial spore densities. Life cycle Dissémination: With the ability to project Fungi are organisms, living beings. They conidia or to grow saprophytically the infect their hosts with spores (conidia) entomopathogenic fungi hâve a limited which germinate on the epidermis. The possibility to actively disseminate. The germ tubes penetrate the skin and en- most important way of dissémination terthe body cavity where multiplication occurs passively via infected hosts, starts. The fungi develop vegetatively other individuals or transportation of as protoplasts, hyphal bodies, hyphae spores in the wind. or yeast-lîke structures called blas- tospores. Most tissues become invad- Metabolites: Metabolites are mainly ed. Some fungi produce metabolites known from Hyphomycetes. Than can which are toxic to the host or compet- be toxic for the host and reduce the ing microorganims. At the end of the incubation time or they can help the parasitic stage the host dies and its body fungus to compete with other microor- is filled with fungal material, either ganisms.

57 WHITE GRUB CONTROL remarks are presented in the following WITH BEAUVERIA sections. BRONGNIARTII WITH REGARD TO REGISTRATION STEPS IN THE DEVELOPMENT OF A The European cockchafer Melolontha MYCOINSECTICIDE melolontha L. (Coleoptera, Scara- baeidae) is a serious pest in many ré­ Strains with the desired characteristics gions of central Europe. A génération must be selected before production can lasts three years. It develops synchro- start. Desired characteristics are mainly nously in outbreak areas resulting in virulence for given hosts, production flights every three years. During the criteria (nutrients, time) and specificity, flight period the adults concentrate at especially absence of adverse effects the borders of forests for about two on vertebrates and plants. Additional weeks. After the feeding/egg matura­ characteristics can include metabolites, tion period the females fly back to their résistance to environmental conditions breeding sites and deposit the eggs in or longevity. Production can take place the soil. The larvae feed on roots of in liquid cultures, on solid média or nearly ail cultivated plants, but most using a combination of both. Produc­ damage is done in grassland. Since the tion must be seen in relation to the final ban of the organochlorinesthere are no product and its application. For aerial longer any registered insecticides for application a liquid product may be best, control of this pest. That is why we while a granule may be best for a soil started a programme to control the treatment. Production parameters can white grubs with the hyphomycete be chosen to produce blastospores, Beauveria brongniartii (Sacc.) Petch. conidia or fungal aggregates. Further- As a first approach we produced blas- more, they can be used to avoid or tospores and treated the swarming suppress production of undesired me­ adults with the aim to use the females tabolites. Additives are used to improve tocarrythepathogen into the soil ofthe or to stabilize the product. Thèse are breeding sites. Two large field trials used for example as wetting or sticking weredone in 1985 and in 1988. Foreach agents, as humefactants and UV pro- trial we treated about 100 ha of forest tectants or as host attractants. Any borders. Secondary effects on honey additive should not hâve adverse ef­ bées, birds, insect and spiders living in fects on organisms. the same enviroment were studied. The production and formulation pro­ Good control of the pest was achieved cess should be followed by a quality after two générations. In a second ap­ control including purity ofthe product proach we developed a product which (foreign microoganisms, undesired could be applied by farmers. This prod­ metabolites) and virulence. A check of uct is based on fungus colonised cereal the genetic identity before and after the grains ("fungus kernels") and has been process gives information on the stabil- registered since 1990 and is presently ity of the fungus. being produced by two companies. The application must be done care- At the beginning of the field expéri­ fully and directed against the target. menta there was no spécifie protocol The use of a fungus against its natural for the registration of microbial control host in the natural environment bears agents. In close collaboration between little risk, while its application against the registration officiais, external spe- non-natural hosts in non-natural envi- cialists and scientists involved in the ronments is problematic (fig. 1) and trials, a registration procédure was increases the possibilities of undesired developed which can be considered as secondary effects. A careful monitoring a good compromise between theoreti- of the trials helps to understand the cal and practical daims. Expériences ecology of the applied fungus and the from this process as well as gênerai interactions with the environment.

58 A • natural host • unnatural host, natural habitat • unnatural host and habitat

10 8 6 4 2

indigenous foreign manlpulated fungal strain

Fig. 1: The needs for the registration of fungal products, indicated by the height of the columns, should be based mainly on the fungal strain and the environment, in which the product is applied.

CRITICAL DOMAINS IN RESPECT TO REGISTRATION

Domain Characters

Fungal species Biology, host range, natural distribution, observations from nature, data from literature Strain Origin (locality, host), virulence, wild strain or genetically altered, genetical characterisation and markers Metabolites Natural and induced metabolites, importance, présence/ absence in product Secondary effects Reactions of humans, other vertebrates and other non-targets, host range, pathogenicity for honey bées and selected bénéficiais

NEEDS FOR SAFE centennarium allowing us to separate EXPLOITATION critical from non-critical species. Nev- ertheless there are enough reasons to subject them to a registration procé­ Entomopathogenic fungi hâve evolved dure. This, however, should be a prag- with the insects hundreds of millions of matic one based on the two principles years ago and are still evolving. They (fig. 1): are part of our natural environment and hâve interacted with humans as long as 1. The registration procédure should be they existed. A lot of knowledge on thèse viewed with regard to the situation interactions has accumulated in the last under which a fungal product is used.

59 2. The doser the use is to the natural time, itallows useofthefungustostudy situation, the less requirements are its ecology and side effects under prac- needed and vice-versa. tical conditions and to answer open questions. It can be withdrawn as soon A few examples are given to illus- as undesired effects are observed. A trate thèse principles: Afungus is known full registration would only be given to produce toxins, but it doesn't make once the required data were presented, sensé to consider thèse if they are not examined and approved. In any case, présent in the final product. If a product close collaboration between involved is applied to the soil, side effects on non researchers, external experts and regis­ hypogeaic organisms should not be tration officiais is proposed. tested. A product based on a soil fun­ gus applied to the soil has to fulfill less requirements than the same product applied in an aerial environment. More ACKNOWLEDGEMENTS examples could be added to demon- strate that the registration procédure The author is greatly indebted to Mark should not be too rigid but be adapt­ Goettel for reviewing the manuscript able to différent situations on a case by and correcting the English phraseolo- case basis. gy- A two step registration procédure is proposed consisting of a provisional and a full registration. A provisional regis­ QUESTIONS tration could be given for low risk use (e.g. fungi applied against their natural 1. Entomopathogenic fungi bear an host in their natural environment). The enormous potential for biocontrol. same but with close limitations ("ex­ Which measures can be taken to périmental permit") could be given for strengthen research on and use of higher risk use (e.g. native fungi ap­ mycoinsecticides? plied against non-natural hosts in non- 2. Should fungi be registered as any natural environments). Genetically al- other entomopathogen, or should tered fungi could get a provisional they be registered according to a registration only after careful examina- particular protocol? tion under quarantine conditions. The advantages of a provisional registra­ 3. Should transgenicfungal mycoinsec­ tion are the following: It is limited in ticides be banned?

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