Deep space and hidden depths: understanding the evolution and ecology of fungal entomopathogens

Entomopathogens are important natural enemies of many insect and mite species and as such have been recognised as providing an important ecosystem service. Indeed, fungal entomopathogens have been widely investigated as biological control agents of pest insects in attempts to improve the sustainability of crop protection. However, even though our understanding of the ecology of fungal entomopathogens has vastly increased since the early 1800s, we still require in-depth ecological research that can expand our scientific horizons in a manner that facilitates widespread adoption of these organisms as efficient biological control agents. Fungal entomopathogens have evolved some intricate interactions with arthropods, plants and other microorganisms. The full importance and complexity of these relationships is only just becoming apparent. It is important to shift our thinking from conventional biological control, to an understanding of an as yet unknown “deep space”. The use of molecular techniques and phylogenetic analyses have helped us move in this direction, and have provided important insights on fungal relationships. Nevertheless, new techniques such as the PhyloChip and pyrosequencing might help us see beyond the familiar fields, into areas that could help us forge a new understanding of the ecology of fungal entomopathogens.     

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

Naturally occurring entomopathogens are important regulatory factors in insect populations. Many species are employed as biological control agents of insect pests in row and glasshouse crops, orchards, ornamentals, range, turf and lawn, stored products, and forestry and for abatement of pest and vector insects of veterinary and medical importance. The comparison of entomopathogens with conventional chemical pesticides is usually solely from the perspective of their efficacy and cost. In addition to efficacy, the advantages of use of microbial control agents are numerous. These include safety for humans and other nontarget organisms, reduction of pesticide residues in food, preservation of other natural enemies, and increased biodiversity in managed ecosystems. As with predators and parasitoids, there are three basic approaches for use of entomopathogens as microbial control agents: classical biological control, augmentation, and conservation. The use of a virus (Oryctes nonoccluded virus), a fungus (Entomophaga maimaiga), and a nematode (Deladenus siricidicola) as innoculatively applied biological control agents for the long-term suppression of palm rhinoceros beetle (Oryctes rhinoceros), gypsy moth (Lymantria dispar), and woodwasp (Sirex noctilio), respectively, has been successful. Most examples of microbial control involve inundative application of entomopathogens. The most widely used microbial control agent is the bacterium Bacillus thuringiensis. The discovery of new varieties with activity against Lepidoptera, Coleoptera, and Diptera and their genetic improvement has enhanced the utility of this species. Recent developments in its molecular biology, mode of action, and resistance management are reviewed. Examples of the use, benefits, and limitations of entomopathogenic viruses, bacteria, fungi, nematodes, and protozoa as inundatively applied microbial control agents are presented. Microbial control agents can be effective and serve as alternatives to broad-spectrum chemical insecticides. However, their increased utilization will require (1) increased pathogen virulence and speed of kill; (2) improved pathogen performance under challenging environmental conditions (cool weather, dry conditions, etc.); (3) greater efficiency in their production; (4) improvements in formulation that enable ease of application, increased environmental persistence, and longer shelf life; (5) better understanding of how they will fit into integrated systems and their interaction with the environment and other integrated pest management (IPM) components; (6) greater appreciation of their environmental advantages; and (7) acceptance by growers and the general public. We envision a broader appreciation for the attributes of entomopathogens in the near to distant future and expect to see synergistic combinations of microbial control agents with other technologies. However, if future development is only market driven, there will be considerable delays in the implementation of several microbial control agents that have excellent potential for use in IPM programs.     

Fungal entomopathogens: new insights on their ecology

An important mechanism for insect pest control should be the use of fungal entomopathogens. Even though these organisms have been studied for more than 100 y, their effective use in the field remains elusive. Recently, however, it has been discovered that many of these entomopathogenic fungi play additional roles in nature. They are endophytes, antagonists of plant pathogens, associates with the rhizosphere, and possibly even plant growth promoting agents. These findings indicate that the ecological role of these fungi in the environment is not fully understood and limits our ability to employ them successfully for pest management. In this paper, we review the recently discovered roles played by many entomopathogenic fungi and propose new research strategies focused on alternate uses for these fungi. It seems likely that these agents can be used in multiple roles in protecting plants from pests and diseases and at the same time promoting plant growth.     

豆野螟的生物防治研究进展与展望

豆野螟Maruca vitrata是豇豆等豆类作物的世界性重要害虫,常年在亚热带地区严重发生,防控难度很大。传统的化学防治方法难以对其进行长久且有效的控制,因而造成害虫抗药性增强、超范围使用化学农药等诸多不良现象,严重威胁人民群众身体健康与生态安全。而生物防治作为减少化学农药用量与残留的关键技术之一,在当前我国绿色农业高速发展期更应引起研究人员的高度重视。因此,本文围绕豆野螟生物防治的研究现状与进展,分别从昆虫性信息素、天敌昆虫资源、昆虫病原物、植物源农药等4个方面进行了概述,并深入探讨了我国豆野螟生物防治领域的研究前景与方向,为豆野螟绿色防控体系的全方位建设提供参考,助力我国绿色农业高质量发展。     

Potential role of microbial pathogens in control of red palm weevil (Rhynchophorus ferrugineus) ‐ A Review

The invasive Red Palm Weevil (RPW), Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae), is one of the most destructive pests of ornamental and economically important palms globally. It has been found in 50 % of date‐growing and 15 % of coconut‐producing countries in the world. Synthetic organic insecticides have been the default method to combat this pest, but they are clearly inefficient due to the secretive nature of the insect and there is concern about non‐target effects from blanket spraying. For this reason, there is increasing interest in biological control methods such as the possible use of microbial entomopathogens, which might be incorporated into IPM approaches. In this review we summarize research work on microbial control agents, their effectiveness against RPW and their integration with other control measures.     

Microbial control of arthropod pests of tropical tree fruits

A multitude of insects and mites attack fruit crops throughout the tropics. The traditional method for controlling most of these pests is the application of chemical pesticides. Growing concern on the negative environmental effects has encouraged the development of alternatives. Inundatively and inoculatively applied microbial control agents (virus, bacteria, fungi, and entomopathogenic nematodes) have been developed as alternative control methods of a wide variety of arthropods including tropical fruit pests. The majority of the research and applications in tropical fruit agroecosystems has been conducted in citrus, banana, coconut, and mango. Successful microbial control initiatives of citrus pests and mites have been reported. Microbial control of arthropod pests of banana includes banana weevil, Cosmopolites sordidus Germar (Coleoptera: Curculionidae) (with EPNs and fungi) among others Oryctes rhinoceros (L.) is one of the most important pests of coconut and one of the most successful uses of non-occluded virus for classical biological control. Key pests of mango that have been controlled with microbial control agents include fruit flies (Diptera: Tephritidae) (with EPNs and fungi), and other pests. Also successful is the microbial control of arthropod pests of guava, papaya and pineapple. The challenge towards a broader application of entomopathogens is the development of successful combinations of entomopathogens, predators, and parasitoids along with other interventions to produce effective and sustainable pest management.     

Insect pathology and fungal endophytes

Fungi that occur inside asymptomatic plant tissues are known as fungal endophytes. Different genera of fungal entomopathogens have been reported as naturally occurring fungal endophytes, and it has been shown that it is possible to inoculate plants with fungal entomopathogens, making them endophytic. Their mode of action against insects appears to be due to antibiosis or feeding deterrence. Research aimed at understanding the fungal ecology of entomopathogenic fungi, and their role as fungal endophytes, could lead to a new paradigm on how to successfully use these organisms in biological control programs.     

Safety of Microorganisms Intended for Pest and Plant Disease Control: A Framework for Scientific Evaluation

Microorganisms are enormous but largely untapped natural resources for biological control of pests and diseases. There are two primary reasons for their underployment for pest or disease control: (1) the technical difficulties of using microorganisms for biological control, owing to a lack of fundamental information on them and their ecology, and (2) the costs of product development and regulatory approvals required for each strain, formulation, and use. Agriculture and forestry benefit greatly from the resident communities of microorganisms responsible for naturally occurring biological control of pest species, but additional benefits are achieved by introducing/applying them when or where needed. This can be done as (1) an inoculative release, (2) an augmentative application, or (3) an inundative application. Because of their specificity, different microbial biocontrol agents typically are needed to control different pests or the same pest in different environments. Four potential adverse effects are identified as safety issues (hazards) associated with the use of microorganisms for the biological control of plant pests and diseases. These are: (1) displacement of nontarget microorganisms, (2) allergenicity to humans and other animals, (3) toxigenicity to nontarget organisms, and (4) pathogenicity to nontarget organisms. Except for allergenicity, these are the same attributes that contribute to the efficacy of microbial biocontrol agents toward the target pest species. The probability of occurrence of a particular adverse nontarget effect of a microbial biocontrol agent may be a function of geographic origin or a specific trait genetically added or modified, but the safety issues are the still the same, including whether the microorganism intended for pest or disease control is indigenous, nonindigenous (imported and released), or genetically modified by traditional or recombinant DNA (rDNA) technology. Likewise, the probability of occurrence of a particular adverse nontarget effect may vary with method of application, e.g., whether as an aerosol, soil treatment, baits, or seed treatment, and may increase with increased scale of use, but the safety issues are still the same, including whether the microorganism is used for an inoculative release or augmentative or inundative application. Existing practices for managing microorganisms in the environment (e.g., plant pathogens,Rhizobium,plant inoculants) provide experience and options for managing the risks of microorganisms applied for pest and disease control. Moreover, experience to date indicates that any adverse nontarget effects, should they occur, are likely to be short-term or transitory effects that can, if significant, be eliminated by terminating use of the microbial biocontrol agent. In contrast, production agriculture as currently practiced, such as the use of tillage and crop rotations, has significant and long-term effects on nontarget organisms, including the intentional and unintentional displacement of microorganisms. Even the decision to leave plant pests and diseases unmanaged could have significant long-term environmental effects on nontarget organisms. Potential safety issues associated with the use of microbial biocontrol must therefore be properly identified and compared with the impact of other options for managing the pest or leaving the pest unmanaged. This paper provides a scientific framework for this process.     

Principles from community and metapopulation ecology: application to fungal entomopathogens

Fungal entomopathogens are often studied within the context of their use for biological control, yet these natural enemies are also excellent subjects for studies of ecological interactions. Here, we present selected principles from community ecology and discuss these in relation to fungal entomopathogens. We discuss the relevance of apparent competition, food web construction, intraguild predation and density-mediated and trait-mediated indirect effects. Although current knowledge of community interactions involving fungal entomopathogens are limited, fungal entomopathogens can be important, interactive members of communities and the activities of fungal entomopathogens should be evaluated in the context of ecological principles. We also discuss aspects of metapopulation ecology and the application of these principles to fungal entomopathogens. Knowledge of ecological interactions is crucial if we are to understand and predict the effects of fungal entomopathogens on host populations and understand the interactions among fungal entomopathogens and other organisms in the communities in which they occur.     

Rapid spread agents may impair biological control in a tritrophic food web with intraguild predation

The augmentation of natural enemies against agricultural pests is a common tactic undertaken to minimize crop damage without the use of chemical pesticides. Failures of this strategy may result from (i) Allee effects acting on biological control agent; (ii) trophic interactions between the released control agent and native species in the local ecosystem; (iii) excessively rapid spreading agents. To investigate the interplay of these mechanisms in pest biocontrol efficiency in the context of intraguild predation (IGP), we develop a one-dimensional dynamical model of a spatial, tritrophic food web with intraguild predation. We show that the agent’s diffusivity (i.e., agent’s dispersal speed), and intraguild predator’s addition of alternative food sources are important factors in determining the success or failure of pest biocontrol. These results are obtained for spatially explicit models by considering the speed of dispersal of the control agent and the pest. Feedback from theoretical models as the one constructed in this work can provide useful guidelines for practitioners in biological control.     

Production and use of biological pest control agents

Biological pest control agents are gaining prominence for the control of insect pests in agriculture and forestry. The shift from chemical control has been due to environmental concerns and recent innovations in biotechnology. Production and use of biological insect control agents is the challenge of the future for pest management.     

Strain improvement of fungal insecticides for controlling insect pests and vector-borne diseases

Insect pathogenic fungi play an important natural role in controlling insect pests. However, few have been successfully commercialized due to low virulence and sensitivity to abiotic stresses that produce inconsistent results in field applications. These limitations are inherent in most naturally occurring biological control agents but development of recombinant DNA techniques has made it possible to significantly improve the insecticidal efficacy of fungi and their tolerance to adverse conditions, including UV. These advances have been achieved by combining new knowledge derived from basic studies of the molecular biology of these pathogens, technical developments that enable very precise regulation of gene expression, and genes encoding insecticidal proteins from other organisms, particularly spiders and scorpions. Recent coverage of genomes is helping determine the identity, origin, and evolution of traits needed for diverse lifestyles and host switching. In future, such knowledge combined with the precision and malleability of molecular techniques will allow design of multiple pathogens with different strategies and host ranges to be used for different ecosystems, and that will avoid the possibility of the host developing resistance. With increasing public concern over the continued use of synthetic chemical insecticides, these new types of biological insecticides offer a range of environmental-friendly options for cost-effective control of insect pests.     

Fungal chitinases and their biological role in the antagonism onto nematode eggs. A review

Chitin, the most abundant aminopolysaccharide in nature, is a rigid and resistant structural component that contributes to the mechanical strength of chitin-containing organisms. Chemically, it is a linear cationic heteropolysaccharide composed of N-acetyl-D-glucosamine and D-glucosamine units. The enzymatic degradation of chitin is performed by a chitinolytic system with synergistic and consecutive action. Diverse organisms (containing chitin or not) produce a great variety of chitinolytic enzymes with different specificities and catalytic properties. Their physiological roles involve nutrition, parasitism, chitin recycling, morphogenesis, and/or defense. Microorganisms, as the main environmental chitin degraders, constitute a very important natural source of chitinolytic enzymes. Nowadays, the most used method for pest and plant diseases control is the utilization of chemical agents, causative of significant environmental pollution. Social concern has generated the search for alternative control systems (i.e., biological control), which contribute to the generation of sustainable agricultural development. Interactions among the different organisms are the natural bases of biological control. Interest in chitinolytic enzymes in the field of biological control has arisen due to their possible involvement in antagonistic activity against pathogenic chitin-containing organisms. The absence of chitin in plants and vertebrate animals allows the consideration of safe and selective “target” molecules for control of chitin-containing pathogenic organisms. Fungi show appropriate characteristics as potential biological control agents of insects, fungi, and nematodes due to the production of fungal enzymes with antagonistic action. The antagonistic interactions between fungi and plant nematode parasites are among the most studied experimental models because of the high economic relevance. Fungi which target nematodes are known as nematophagous fungi. The nematode egg is the only structural element where the presence of chitin has been demonstrated. In spite of being one of the most resistant biological structures, eggs are susceptible to being attacked by egg-parasitic fungi. A combination of physical and chemical phenomena result in their complete destruction. The contribution of fungal chitinases to the in vitro rupture of the eggshell confirms their role as a pathogenic factor. Chitinases have been produced by traditional fermentation methods, which have been improved by optimizing the culture conditions for industrial processes. Although wild-type microorganisms constitute an alternative source of chitinolytic enzymes, the advances in molecular biology are allowing the genetic transformation of fungi to obtain strains with high capability as biocontrol agents. Simultaneously, a better understanding of rhizosphere interactions, additional to the discovery of new molecular biology tools, will allow the choosing of better alternatives for the biological control of nematodes in order to achieve an integrated management of the soil ecosystem.     

Local adaptation to biocontrol agents: A multi-objective data-driven optimization model for the evolution of resistance

Spatial and temporal variability in the application of biological control agents such as parasites or pathogenic bacteria can cause the evolution of resistance in pest organisms. Because biocontrol will be more effective if organisms are not resistant, it is desirable to examine the evolution of resistance under different application strategies.We present a computational method that integrates a genetic algorithm with experimental data for predicting when local populations are likely to evolve resistance to biocontrol pathogens. The model incorporates parameters that can be varied as part of pest control measures such as the distribution and severity of the biocontrol agent (e.g., pathogenic fungi). The model predicts the evolution of pathogen defense as well as indirect selection on several aspects of the organism's genetic system. Our results show that both variability of selection within populations as well as mean differences among populations are important in the evolution of defenses against biocontrol pathogens. The mean defense is changed through the pest organism's genotype and the variance is affected by components of the genetic system, namely, the resiliency, recombination rate and number of genes.The data-driven model incorporates experimental data on pathogen susceptibility and the cost of defense. The results suggest that spatial variability rather than uniform application of biological control will limit the evolution of resistance in pest organisms.     

Plant volatiles: new perspectives for research in Brazil

Agroecosystems consist on complex trophic relationships among host plants, herbivores and their natural enemies. This article reviews the research of plant volatiles in Brazil, in order to determine multiple resistance mechanisms of economically important crops and to contribute to the understanding of insect-plant interactions. Most pest management programs, including chemical and biological control, do not consider the impact of these chemicals on herbivores and their natural enemies. Alternative control methods are being developed in order to improve our understanding on the endogenous mechanisms of plant induced defenses against phytophagous arthropods. The use of plant volatiles technology as an additional tool in integrated pest management programs would offer a new and environmentally sound approach to crop protection. This technique involves the development of baits that attract beneficial organisms and the manipulation of biochemical processes that induce and regulate plant defenses, key factors in the improvement of control programs against economically important pests. The elucidation of the mechanisms involved in the indirect defenses of plants will result in useful tools for biological control of crop pests.     

稻飞虱天敌螯蜂研究进展

稻飞虱（褐飞虱Nilaparvata lugens、白背飞虱Sogatella furcifera、灰飞虱Laodelphax striatellus）是世界性重要的水稻Oryza sativa L.害虫之一,给水稻生产造成了重大经济损失。化学防治一直是控制稻飞虱的主要途径,但长期使用化学药剂使稻飞虱产生抗药性,并引起害虫增殖等诸多弊端,迫切需要有效的生物防控手段进行控害。螯蜂是稻飞虱若虫和成虫期重要天敌,兼具捕食与寄生的双重习性,在控制稻飞虱种群数量方面发挥着重要的作用,然而,国内外有关螯蜂的研究报道仍然偏少。本文综述了我国稻飞虱天敌螯蜂常见种类、生物学特性、控害效果及其影响因子,分析了存在的问题,旨在为进一步开发利用螯蜂资源提供参考。     

Current developments in microbial control of insect pests and prospects for the early 21st century

The role of microbial control in crop and forest protection and the abatement of insects of medical and veterinary importance has expanded considerably with the discovery and development of new microbial control agents and genetic improvement in bacterial and viral pathogens, and improvements in formulation, application options and compatibility with other interventions. A synopsis of the literature regarding the current use of bacteria, viruses, fungi, protozoans and nematodes as microbial control agents is presented along with speculation on their potential in the early 21st century. The most widely used of all microbial control agents isBacillus thuringiensis. The isolation within the past two decades of new strains that are larvicidal for certain Diptera and Coleoptera has increased the utility of the bacterium considerably. Further improvements in efficacy and broadening of its host range are in progress with the isolation of strains with new toxins and the manipulation ofB. thuringiensis genes that encode toxin production using both recombinant and nonrecombinant methods. Genetic manipulation of these genes has also enabled their incorporation into crop plants. The development and commercial availability of entomopathogenic nematodes in the families Steinernematidae and Heterorhabditidae expands the options for the control of insects, especially those with soil inhabiting stages. The results of natural epizootics of fungi and viruses often obviate the requirement for additional interventions. Breakthroughs in understanding the genetics ofBaculovirus and subsequent gene manipulation have increased their virulence and utility. Improved production methods that utilize insect cell culture technology may enable affordable use ofBaculovirus in the not too distant future. Fungi continue to offer the only control options using entomopathogens against plant sucking insects. Although fungi have great potential for development as microbial control agents, only a few have been used on an operational scale. Some factors that might limit the full range of entomopathogen potential, including development of resistance, are discussed. Because of their selectivity and minimal environmental impact, microbial control agents will be ideal components of integrated pest management programs in the early 21st century and beyond. However, if they are used merely as replacements for chemical pesticides, then eventually these agents will face some of the same fate as the chemicals they replace, particularly with respect to resistance.     

Interspecific extrinsic and intrinsic competitive interactions in egg parasitoids

Interspecific competitive interactions can occur either between adult parasitoids searching/exploiting hosts (extrinsic competition) or between parasitoid larvae developing within the same host (intrinsic competition). Understanding how interspecific competition between parasitoids can affect pest suppression is important for improving biological pest control. The purpose of this work was to review both extrinsic and intrinsic competition between egg parasitoid species. These are organisms that are often candidates for biological control programs due to their ability to kill the pest before the crop feeding stage. We first reviewed the literature about interspecific competitive abilities of adult parasitoids in terms of comparative host location strategies highlighting which ecological and behavioral factors are likely to shape extrinsic competition. Then we focused on the interspecific competitive interactions between immatures developing within the same host taking into account which factors play a key role in the outcome of intrinsic competition. Finally we conclude stressing on the need to elucidate the overall competitive interaction that parasitoid species may experience in the field in order to enhance biological control success.     

我国梨小食心虫综合防治研究进展

近年来,由于农业产业结构的调整,我国北方果树栽培种类日益增多、种植面积不断扩大。重要果树害虫梨小食心虫Grapholitha molesta(Busck)为害大幅回升、危害逐年增加。针对这一情况,在西北、东北和华北3个北方果树生产代表区域建立50余个监测示范点,开展了梨小食心虫的生物生态学规律及综合防治技术的研究、集成与示范。研究结果表明,气候变化和种植结构对梨小食心虫发生规律有显著影响。全球气候变暖条件下,梨小食心虫年发生世代呈增加趋势;在果树混栽区域,晚熟桃为梨小食心虫的主要越冬场所。防治技术方面,在对梨小食心虫常规农业防治、物理防治、生物防治、化学防治技术组装配套的基础上,重点开展了高效节水诱捕器、国产迷向产品研发及标准化应用技术、优势天敌饲养及释放技术、专用农药研发及农药减量化技术等研究工作。前瞻性地研发了植物源诱捕剂及迷向新剂型等贮备技术。最后针对当前梨小食心虫防治工作中存在的问题和不足,确定了下一步的研究方向:(1)全球气候变暖对梨小食心虫发生动态的影响;(2)梨小食心虫成虫不同寄主间的转移规律;(3)梨小食心虫的抗性监测技术和快速诊断试剂盒研制;(4)梨小食心虫的抗性分子机理与抗性治理技术。     

Biocoenology and control of whiteflies in sericulture

Abstract The damage caused by the whiteflies Dialeuropora decempuncta (Quaintance & Baker, 1913), Aleurodicus dispersus Russell, and Aleuroclava sp. to mulberry plants is extensive and they cause a huge economic loss to mulberry leaves which affects silkworm rearing. Dialeuropora decempuncta is a major pest in western Bengal, whereas spiralling whitefly A. dispersus has been reported to attack mulberry plants in South India. The whiteflies are present throughout the year in south India, with high populations in summer (March—June) and low ones in winter (October—January). The population is positively correlated with temperature and negatively correlated with humidity. Chemical control is the quick solution to minimize the pest population. However, the indiscriminate and large-scale use of highly poisonous synthetic chemical pesticides has resulted in ecological imbalance, in addition to their toxic effects on living organisms, including human beings. Hence there is a need for developing methods and materials within an eco-friendly atmosphere. Previous investigations indicate that neem-based insecticides may be a suitable alternative for pest management in sericulture. Use of neem products in sericultural pest control has many merits. It will also help in the successful introduction of biological controls in India. Several exotic parasitoids have been found to be highly effective, including two aphelinid parasitoids Encarsia haitiensis Dozier and E. meritoria Gahan. These are most promising and are reported to minimize the fly pest population. The parasitization potential and behaviour of the parasitoids have to be carefully assessed before they are introduced to control fly pest populations. There is a need for careful assessment of all these advanced biological technologies in order to develop a profitable, safe and durable approach for whitefly control in sericulture.