Organizmy pożyteczne w strategiach biologicznego zwalczania – grzyby owadobójcze

The 6/04 standard of the European and Mediterranean Plant Protection Organisation (EPPO) on the safe use of biological control is a decision-support scheme (DSS) for the import and release of biological control agents in Europe. It was recently developed by the Joint EPPO/International Organisation of Biological Control (IOBC) Panel on Biological Control Agents. The DSS can be used to assess the potential environmental impacts of biological control agents. It is valid for different types of biological control: classical and augmentative biological control of invertebrates, pathogens and weeds. However, the DSS is not yet widely implemented in Europe and, during preliminary trials, it was found that its broad range of usages could lead to some confusion or misunderstandings, as well as requiring unnecessary information in some cases. Thus, the scheme was modified to specifically assess classical biological control against plant pests, i.e. the introduction of exotic natural enemies of plant pests for establishment and long-term control. The new version of the scheme was then tested on two parasitoids that are presently being released in Europe, the figitid Ganaspis cf. brasiliensis against the spotted wing drosophila Drosophila suzukii and the mymarid Cleruchoides noackae against the Eucalyptus bronze bug Thaumastocoris peregrinus. Both parasitoids were successfully assessed with the new version of the DSS. No major issues were encountered during the assessments and most questions were answered with low levels of uncertainty. Both assessments concluded that the parasitoids were safe to release in the impact assessment areas, with positive impacts exceeding negative impacts. Suggestions for potential improvements are provided.

Opinions about the value of biological control are often extreme. Colloquially, biological control most often refers to classical biological control, in which one species is introduced from another region to control pests such as arthropod herbivores in agricultural systems, or weeds in managed and natural systems.1 As such, biological control has the potential to be a low-cost, chemical free, means to control pests. Numerous biological control programs have been unqualified successes (Bellows 2001), such as the control of cacti in Australia with the moth Cactoblastis cactorum (Raghu and Walton 2007), of cottony-cushion scale (Icerya purchasi) in California with the vedalia lady beetle, Rodolia cardinalis (Caltagirone and Doutt 1989), and of glassy-winged sharpshooters in French Polynesia with the egg parasitoid Gonatocerus ashmeadi (Grandgirard et al. 2009). Yet, classical biological control, as with any introduction of a species into a new area, necessarily involves the unknown and therefore carries some inherent risk (Simberloff and Stiling 1996) – what will these organisms actually do in a novel ecosystem? The most unpredictable element in biological control is the extent to which the realized niche is modified in the new environment. This effect has been responsible for some disastrous outcomes of classical biological control, many of which occurred during an era when vertebrates were being introduced around the world by Europeans for a variety of reasons (e.g., introducing the birds of Shakespeare to America, Mirsky 2008), including for biological control (Howarth 1991). The introductions as biological control agents of cane toad to Australia (Crossland et al. 2000) and mongoose to Hawaii (Hays and Conant 2007) are notorious. Introductions of generalist invertebrate agents also have had dire consequences, such as the introduction of predatory snails to French Polynesia (Murray et al. 1988; Coote 2007). In retrospect, some of the unintended consequences of biological control could have been avoided with more ecological knowledge (McEvoy and Coombs 2000) or more societal appreciation for native species (which has developed with time, Henneman and Memmott 2001), but with other introductions, it would have been impossible to know ahead of time what the risks would be (e.g., gall fly agents of knapweeds providing supplementary food to mice that harbor hantavirus, Pearson and Callaway 2006). Many of the unknown outcomes of biological control are purely ecological – what is the risk that a wasp, introduced to parasitize an agricultural pest, will also be able to feed on a native insect? Other unknowns involve evolution – will a herbivore adapt over time to be able to feed on a new nontarget host or hybridize with a closely related species? This volume explores the evolutionary aspects of biological control. Although often overlooked, evolutionary considerations are critical to all stages of classical biological control, from agent selection, to quarantine, release, establishment, and ultimately success in pest control (Ehler et al. 2004). Many questions are unresolved. For example, should agents be chosen that have a long history with the host or are ‘new associations’ more likely to succeed (Hokkanen and Pimentel 1989)? Can one improve effectiveness through artificial selection (Hopper et al. 1993)? Will postcolonization adaptation of the agent increase the likelihood of success, and/or are hosts equally likely to evolve resistance over time (Roderick 1992; Holt and Hochberg 1997; Hufbauer 2001)? Are generalist consumers more likely to survive in novel environments or are specialists more effective (Murdoch et al. 1985; Waage 1990; Brodeur 2012)? More recently, concern for the environment, as well as theory examining the reasons for success of generalist predators, prompted a shift to the release of specialized consumers typically preceded by extensive testing aimed at delimiting the host range of candidate biological control agents. While this approach has clearly made biological control more predictive ecologically, research focused on host range currently lacks measures of genetic variation in host use and responses of those hosts, and thus evolutionary uncertainties remain.

Parasitoid wasps as effective biological control agents

Preface. Acknowledgments. Contributors. Part 1: Perspectives. 1. Critical Issues Related to Nontarget Effects in Classical Biological Control of Insetcs L.E. Ehler. 2. Nontarget Effects of Biological Control: What Are We Trying to Miss? J.A. Lockwood. 3. The Frequency and Strength of Nontarget Effects of Invertebrate Biological Control Agents of Plant Pests and Weeds P. Stiling, D. Simberloff. 4. The Impact of Nontarget Concerns on the Practice of Biological Control R.H. Messing. Part 2: Parasitoids and Predators. 5. Predicting the Risk from Biological Control Agent Introductions: A New Zealand Approach B. Barratt, et al. 6. Parasitoid Drift in Hawaiian Pentatomoids P.A. Follett, et al. 7. Evaluating Nontarget Effects of Classical Biological Control: Fruit Fly Parasitoids in Hawaii as a Case Study J.J. Duan, R.H. Messing. 8. Trichogramma Nontarget Impacts: A Method for Biological Control Risk Assessment D.B. Orr, et al. 9. Coccinellid Introductions: Potential for and Evaluation of Nontarget Effects J.J. Obrycki, et al. 10. Food Webs as a Tool for Studying Nontarget Effects in Biological Control J. Memmott. Part 3: Weeds. 11. Why Things Bite Back: Unintended Consequences of Biological Weed Control P.B. McEvoy, E.M. Coombs. 12. Importation Protocols and Risk Assessment of Weed Biological Control Agents in Australia: The Example of Carmenta nr ithacae T. Withers, et al. 13. Negative Ecological Effects of the Musk Thistle Biological Control Agent, Rhinocyllus conicus S.M. Louda. 14. Biological Control of Musk Thistle: A Reassessment J.R. Nechols. Part 4: Pathogens. 15. Predicting the Host Range of Entomopathogenic Fungi A.E. Hajek, L. Butler. 16. Monitoring the Effects of Bacillus thuringiensis kurstaki on Nontarget Lepidoptera in Woodlands and Forests of Western Oregon J.C. Miller. 17. Environmental Impacts of Entomopathogenic Nematodes Used for Biological Control in Soil M. Barbercheck, L.C. Millar. Index.

Living organisms are used as biological pest control agents in (i) classical biological control, primarily for permanent control of introduced perennial weed pests or introduced pests of perennial crops; (ii) augmentative biological control, for temporary control of native or introduced pests of annual crops grown in monoculture; and (iii) conservative or natural control, in which the agroecosystem is managed to maximize the effect of native or introduced biological control agents. The effectiveness of biological control can be improved if it is based on adequate ecological information and theory, and if it is integrated with other pest management practices.

Metabarcoding is revolutionizing fundamental research in ecology by enabling large-scale detection of species and producing data that are rich with community context. However, the benefits of metabarcoding have yet to be fully realized in fields of applied ecology, especially those such as classical biological control (CBC) research that involve hyperdiverse taxa. Here, we discuss some of the opportunities that metabarcoding provides CBC and solutions to the main methodological challenges that have limited the integration of metabarcoding in existing CBC workflows. We focus on insect parasitoids, which are popular and effective biological control agents (BCAs) of invasive species and agricultural pests. Accurately identifying native, invasive and BCA species is paramount, since misidentification can undermine control efforts and lead to large negative socio-economic impacts. Unfortunately, most existing publicly accessible genetic databases cannot be used to reliably identify parasitoid species, thereby limiting the accuracy of metabarcoding in CBC research. To address this issue, we argue for the establishment of authoritative genetic databases that link metabarcoding data to taxonomically identified specimens. We further suggest using multiple genetic markers to reduce primer bias and increase taxonomic resolution. We also provide suggestions for biological control-specific metabarcoding workflows intended to track the long-term effectiveness of introduced BCAs. Finally, we use the example of an invasive pest, Drosophila suzukii, in a reflective "what if" thought experiment to explore the potential power of community metabarcoding in CBC.

Next generation biological control – an introduction

The USA has been actively involved in classical biological control projects against invasive insect pests and weeds since 1888. Classical (importation) biological control relies upon natural enemies associated through coevolution with their target species at their geographic origin to also provide long-term, self-sustaining management where the pest/weed has become invasive. Biological control agents are a form of genetic resources and fall under the purview of the 1993 Convention on Biological Diversity (CBD) and its Nagoya Protocol (NP), which entered into force in 2014 to address equitable sharing of benefits arising from utilization of genetic resources. Safe and effective classical biological control agents have historically been shared among countries experiencing problems with invasive species. However, a feature of the Nagoya Protocol is that countries are expected to develop processes governing access to their genetic resources to ensure that the benefits are shared equitably-a concept referred to as "access and benefitsharing" (ABS). Although the USA is not party to the CBD nor the NP, US biological control programs are affected by these international agreements. Surveying, collecting, exporting and importing of natural enemies may be covered by new ABS regulatory processes. Challenges of ABS have arisen as various countries enact new regulations (or not) governing access to genetic resources, andthe processes for gaining access and sharing the benefits from these resources have become increasingly complex. In the absence of an overarching national US policy, individual government agencies and institutions follow their own internal procedures. Biological control practitioners in the USA have been encouraged in recent years to observe best practices developed by the biological community for insect and weed biological control.

The movement of humans around the earth has been associated with an amazing redistribution of a variety of organisms to new continents and exotic islands. The natural biodiversity of native communities is threatened by new invasive species, and many of the most serious insect and weed pests are exotics. Classical biological control is one approach to dealing with nonindigenous species. If introduced species that lack natural enemies are competitively superior in exotic habitats, introducing some of their predators (herbivores), diseases, or parasitoids may reduce their population densities. Thus, the introduction of more exotic species may be necessary to reduce the competitive superiority of nonindigenous pests. The intentional introduction of insects as biological control agents provides an experimental arena in which adaptations and interactions among species may be tested. We can use biological control programs to explore such evolutionary questions as: What characteristics make a natural enemy a successful biological control agent? Does coevolution of herbivores and hosts or predators (parasitoids) and prey result in few species of natural enemies having the potential to be successful biological control agents? Do introduced natural enemies make unexpected host range shifts in new environments? Do exotic species lose their defense against specialized natural enemies after living for many generations without them? If coevolution is a common force in nature, we expect biological control interactions to demonstrate a dynamic interplay between hosts and their natural enemies. In this chapter, I consider biological control introductions to be experiments that might yield evidence on how adaptation molds the interactions between species and their natural enemies. I argue that the best biological control agents will be those to which the target hosts have not evolved resistance. Classical biological control is the movement of natural enemies from a native habitat to an exotic habitat where their host has become a pest. This approach to exotic pests has been practiced since the late 1800s, when Albert Koebele explored the native habitat of the cottony cushion scale, Icrya purchasi, in Australia and introduced Vadalia cardinalis beetles (see below) to control the cottony cushion scale on citrus in California. This control has continued to be a success.

Insect Pathogens as Biological Control Agents: Do They Have a Future?

Biological control of insect pests consists of the beneficial action of entomophagous predators and parasitoids, and entomopathogenic microorganisms (protozoa, nematodes, bacteria, fungi, and viruses) in controlling pest populations. There are three biological pest control strategies: classical biological control, conservation, and augmentation. Because Rhynchophorus ferrugineus (red palm weevil, RPW) and Paysandisia archon (palm borer moth, PBM) are invasive species in a large area, it could be hypothesized that the only feasible and suitable biocontrol method is classical biological control, defined as “the intentional introduction of an exotic biological control agent for permanent establishment and long-term pest control” (Eilenberg, Hajek, and Lomer 2001). Unfortunately, there are few reports on parasitoids and predators of these two palm pests in their native areas, probably because they do not cause important damage in those areas. RPW eggs, larvae, and adults are preys of the black earwig Chelisoches morio (Fabr.) (Dermaptera: Chelisochidae). The common blackbird (Turdus merula L.), the common kestrel (Falco tinnunculus L.), and the common magpie (Pica pica L.) have also been described to feed on adults and larvae of PBM and RPW. In addition, some mammals, such as bats and rats, can be occasional predators of adults of both the weevil and the moth. However, the practical use of mammals, reptiles, and birds in classical biological control is limited. There is some parasitization of R. ferrugineus larvae by the large wasp Scolia erratica Smith and by the calliphorid fly Sarcophaga fuscicauda Bottcher, but again, they do not play a significant role in limiting the pest populations. Laboratory experiments performed with several strains of Trichogramma have shown this parasitoid's potential for PBM egg control. Among entomopathogenic microorganisms, the bacteria Bacillus thuringiensis (Berliner) and Pseudomonas aeruginosa (Schroeter) showed low activity against RPW larvae in laboratory assays. An unidentified species of the cytoplasmic polyhedrosis virus group has been reported to infect all stages of RPW, with laboratory infections of late instars resulting in the development of malformed adults. Natural infections of RPW by the genera Heterorhabditis and Steinernema have been occasionally recorded, but inundative release of commercial strains of Steinernema carpocapsae (Weiser) (Nematoda: Steinernematidae) produced inconsistent data. Recent studies have revealed the natural occurrence of entomopathogenic fungi in weevil and moth populations throughout the Mediterranean Basin, and the efficacy of several indigenous strains of Beauveria sp. and Metarhizium sp. against larvae of both species and adults of RPW has been ascertained under laboratory and field conditions using different approaches. (Resume d'auteur)

Biological control involves the deliberate introduction of natural enemies for the control of pest organisms, including insects, weeds and diseases.A general difference exists between augmentative releases where biological control agents are used periodically, i.e. once or several times within a season, and classical biological control where agents are released with the aim of establishment and, ideally, a permanent pest control.Whereas native candidates are generally given preference in augmentative biological control, in some cases exotic species have been used. By contrast, for classical biological control the rule is that exotic natural enemies are introduced for the control of exotic pests. Pest species may either interfere with agricultural production without being invasive per se or may be invasive on a larger scale, thereby threatening ecosystems and natural reserves. Whereas arthropod biological control generally applies to the former, it is in the weed control section that biological control agents are often released to control invasive species. This means that biological control finds itself in the unique position of being both an important strategy for the control of alien invasive species and also a route by which potentially damaging new alien species (i.e. the natural enemies) are themselves introduced and spread (Chap. 2). This chapter will briefly review the positive aspects of biological control and will highlight a few examples. It will further review negative aspects of biological control introductions. One of the examples where biological control led to detrimental environmental effects was the introduction of the ladybeetle Harmonia axyridis, and this case will be outlined in more detail. This example will also be used to explore some of the population biology mechanisms which can contribute to the net effects of introduced natural enemies. Finally, some information on recent developments and improvements in risk assessment of biological control agents is provided.

SummaryClassical biological control remains the only tool available for permanent ecological and economic management of invasive alien species that flourish through absence of their co‐evolved natural enemies. As such, this approach is recognized as a key tool for alien species management by the Convention on Biological Diversity (CBD), the European and Mediterranean Plant Protection Organization (EPPO) and the European Strategy on Invasive Alien Species (ESIAS). Successful classical biological control programmes abound around the world, despite disproportionate attention being given to occasional and predictable non‐target impacts. Despite more than 130 case histories in Europe against insect pests, no exotic classical biological control agent has been released in the EU against an alien invasive weed. This dearth has occurred in the face of increasing numbers of exotic invasive plants being imported and taking over National Parks, forests and amenity areas in this region, as well as a global increase in the use of classical biological control around the world. This paper reviews potential European weed targets for classical biological control from ecological and socioeconomic perspectives using the criteria of historical biological control success, taxonomic isolation from European native flora, likely availability of biological control agents, invasiveness outside Europe and value to primary industry and horticulture (potential for conflicts of interest). We also review why classical biological control of European exotic plants remains untested, considering problems of funding and public perception. Finally, we consider the regulatory framework that surrounds such biological control activities within constituent countries of the EU to suggest how this approach may be adopted in the future for managing invasive exotic weeds in Europe.

Establishment of classical biological control targeting emerald ash borer is facilitated by use of insecticides, with little effect on native arthropod communities

El Centro para el Control Biológico en Centro América (CCBCA) fue creado en 1989 por la Escuela Agrícola Panamericana, financiado por la United States Agency for International Development (USAID) en Honduras. El CCBCA se enfocó en el control biológico clásico, el aumento y la conservación de enemigos naturales. En el 2000 cambió el nombre de Laboratorio de Control Biológico y se enfocó en el aprender haciendo de los estudiantes de la Escuela Agrícola Panamericana y la producción y comercialización de enemigos naturales de plagas agrícolas. El único parasitoide conocido que ataca al picudo de las bromelias (Metamasius quadrilineatus), fue encontrado en las investigaciones del CCBCA; resultó una especie nueva nombrada Lixadmontia franki que fue liberada en Florida en el 2007 para el control biológico del picudo mejicano de las bromelias (Metamasius callizona). Se determinaron los organismos parasíticos de las plagas Plutella xylostella, Mocis latipes, Spodoptera frugiperda, Leptophobia aripa y Liriomyza spp. Cuatro especies de avispas parasíticas exóticas, un baculovirus, un hongo y tres picudos fueron introducidos a Honduras para control biológico clásico: Cotesia plutellae (parasitoide asiático de P. xylostella); Diadromus collaris (parasitoide pupal de P. xylostella); Telenomus remus (parasitoide que ataca a los huevos de 30 especies de lepidópteros); una especie de Eretmocerus (originaria de India, para controlar Bemisia tabaci); los picudos Neochetina bruchi y Neochetina eichhorniae y el hongo Cercospora piaropi (para el control de la maleza acuática lirio de agua (Eichhornia crassipes); y el picudo Neohydronomous affinis (controlador biológico de la maleza acuática lechuga de agua (Pistia stratiotes). En el 2000, Zamorano cambió la estrategia del uso de control biológico y empezó a incursionar en la producción comercial de microrganismos para el control de plagas, debido a una demanda no satisfecha. Los controladores biológicos que ha producido son el hongo antagonista Trichoderma harzianum (Trichozam™) para combatir hongos en el suelo, Beauveria bassiana (Bazam™) para controlar lepidópteros y coleópteros, Lecanicillium lecanii (Verzam™) para el control de áfidos y mosca blanca, Metarhizium anisopliae (Metazam™) para el control de salivazo (Aeneolamia spp.) y larvas de coleópteros en caña de azúcar, y Purpureocillium lilacinum (Pazam™) para controlar nematodos. Además, ha reproducido y vendido la chinche depredadora Orius insidiosus para el control de trips, áfidos y mosca blanca, el ácaro depredador Neoseiulus longispinosus para el control de la arañita roja (Tetranychus spp.) y el nematodo entomófago Heterorhabditis bacteriophora para el control de insectos del suelo, especialmente contra Phyllophaga spp., Cosmopolitus sordidus, larvas de lepidóptera, picudo del camote (Cylas formicarius) y termitas en el suelo. Posiblemente, el mayor aporte es en la enseñanza de las técnicas y tecnologías del control biológico de plagas que se han distribuido por América Latina a través de los graduados de Zamorano que estudiaron y fueron entrenados en Zamorano.DOI: http://dx.doi.org/10.5377/ceiba.v52i1.966