Environmental and public health problems arising from the use of chemical insecticides have led to an increasing demand for alternatives for insect pest control. Together with this, widespread public concern resulting in governmental bans on many of the most effective insecticides and development of insecticide resistance has severely reduced the range of useful insecticides available. Alternative control measures such as the biological control of pest insects with parasitoids and predators and microbial biocides have been in field use for several decades. Although these alternatives are being continually improved, most insect pests are nonetheless still controlled with chemical insecticides.
This book presents the latest work on the biological control of insects using nematodes; it covers a range of topics that will help provide a better understanding of the potential problems involved in developing these nematodes as biological control agents. Nematodes infect hundreds of different species from most orders of insects and affect their insect hosts in a variety of ways.
- Page 1Abstract
Insect nematology is emerging as a major discipline within insect pathology and biological control. Interest in insect nematology can be attributed to (1) the successful use of nematodes in biological control of insect pests, (2) the ready availability of some nematode species for classical biological control, integrated pest management (IPM) and inundative or inoculative release programmes against major insect pests, and (3) the need to find alternative control tactics for chemical insecticides. Although there are eleven nematode families which offer potential for the biological control of insects, the recent focus has been on five families. Specifically, they are Mermithidae in the class Adenophorea and Phaenopsitylcnchidae (formerly Neotylenchidae), Aphelenchoididae, Stcinerncmatidae, and Heterorhabditidae in the class Secernentea.
Nematodes infect hundreds of different species from most orders of insects and affect their insect hosts in a variety of ways. Some insect-parasitic nematodes have little or no detectable effect on their hosts, whereas others reduce fecundity or cause sterility, reduce longevity, reduce flight activity, or delay development. There may also be other behavioural, physiological or morphological aberrations. Some insect parasitic nematodes such as mermithids eventually kill their hosts. In contrast, the entomopathogenic nematodes, Steinernema and Heterorhabditis, rapidly kill their hosts because of their associations with mutualistic bacteria of the genus Xenorhabdus. Thus, the insect-parasitic nematodes have been primarily utilised as classical biological control agents and the entomopathogenic nematodes are largely used as biological insecticides.
- Page 11Abstract
A recent outbreak of the woodwasp Sirex noctilio in the ‘Green Triangle’ of Southern Australia where the nematodes had not been adequately introduced resulted in up to 80% tree death in some areas of the 50 000 hectares of Pinus radiata plantations. The outbreak served as a ‘control block’ to compare with other areas of Southern Australia that had adequate nematode dispersal and usually insignificant tree mortality. If not controlled, over a 30 year rotation of Australia’s 1 million hectares of pines, sirex has the potential to cause a $1–$4 billion loss of timber. The nematode, Deladenus siricidicola, sterilises female sirex during its parasitic cycle but also has multiple free-living cycles in the tree while feeding on the symbiotic fungus, Amylostereum areolatum. The fungal cycle enables unlimited in vitro culture of this nematode for biological control. Inadvertently, persistent use of this cycle has selected for a marked decline in infectivity and reduced levels of parasitism in sirex both from timber inoculated for liberation programs and in sirex from the field. This situation is now being remedied following the re-isolation of the strain from where it was liberated 20 years ago and a technique for indefinite storage of the strain in liquid nitrogen has been developed. The determination of the mechanism for the switch from one cycle to the other has enabled the development of techniques to check on the infectivity of nematodes collected from the field.
- Page 21Abstract
Agamermis unka, a mermithid parasite of the brown planthopper (BPH) Nilaparvata lugens, occurs naturally in Korea. The biology of this nematode follows a typical mermithid life cycle with the preparasite emerging from the egg, crawling up the rice stem, parasitising BPH by direct penetration through the host’s cuticle, and killing the host upon emergence as a postparasite. It overwinters in the soil and mates between May and August. A number of factors affect the rate of parasitism of BPH by A. unka. Brachypterous adult and female BPHs show a significantly higher proportion of parasitised individuals than macropterous adult and male BPHs. The closer proximity of the short-winged forms to the surface of the water accounts for the higher rates of parasitism, but the reason for the difference between the sexes is unknown. Tilled rice fields have a higher proportion of BPH parasitised by the mermithid than unfilled fields. Similarly, irrigated rice fields show higher rates of parasitism than unirrigated fields. However, if sufficient rainfall occurs, there is no difference in parasitism. Insecticide application, particularly carbofuran, adversely affects mermithid parasitism of BPH. This information provides a background for the development of an integrated pest management program for BPH.
- Page 27Abstract
Noctuidonema guyanense is a newly described ectoparasitic nematode that attacks the moth stage of Spodoptera frugiperda (I.E. Smith) and a few other related noctuid species. Its distribution is limited to the tropical and subtropical Americas. Moths harbouring N. guyanense exhibit cuticular aberrations and subcuticular muscular deterioration beneath nematode positions. Infestation of S. frugiperda by N. guyanense is limited mostly to a host’s abdomen. In the laboratory, N. guyanense reduces survival in moths of both sexes, longevity in males, and viability of eggs laid by infested S. frugiperda females.
- Page 33Abstract
Enlomopathogenic nematodes are being used to control some major tree borer pests in China. Holcocerus insularis, a serious pest of shade trees and Chinese hawthorn in northern China, and Zeuzera multistrigata, a serious pest of Casuarina equisetifolia in southern China, were shown to be susceptible to Steinernema carpocapsae. Determination of appropriate environmental conditions and techniques for application of the nematodes led to S. carpocapsae being used more effectively and more economically than pesticide for controlling this pest. This information was disseminated to local authorities through workshops, demonstrations and the distribution of sample packs of the nematodes. Several Landscape Bureaux of major cities have adopted the use of entomopathogenic nematodes as the standard means of controlling H. insularis.
- Page 41Abstract
A system developed for managing Cosmopolites sordidus populations by introducing entomopathogenic nematodes into bait holes made in residual banana corms has proved promising in large scale field trials. Of 32 different strains and species of Steinernema and Heterorhabditis tested, the BW strain of Steinernema carpocapsae was the most infectious to adult C. sordidus. Although 250 000 infective juveniles of this nematode were needed per bait hole to produce high levels of mortality in adults, this was economically feasible. In addition to providing a means of managing C. sordidus despite increasing levels of resistance to organophosphorus insecticides, the use of entomopathogenic nematodes instead of insecticides can reduce soil erosion, acidification and, salinity by enabling mulching to be used.
- Page 49Abstract
White grubs, the larvae of scarab beetles, are serious pests of turf, pastures, sugar cane, and horticultural crops throughout the world. Several nematode species (Steinernema glaseri, S. anomali, S. kushidai, and Heterorhabditis megidis) and strains of S. carpocapsae and H. bacteriophora have been isolated from white grubs, indicating their potential to control scarab larvae. Early efforts to use S. glaseri against the Japanese beetle failed, possibly due to a lack of appreciation for the nematode-bacterium complex. More recently, field efficacy with S. glaseri and H. bacteriophora has been demonstrated against a variety of white grubs. However, before reliable results can be expected, more information on overcoming host defence mechanisms is essential, application techniques which allow nematodes to reach target pests must be developed, and the effects of biotic and abiotic factors on nematode survival in the soil environment require elucidation. Prospects are increasing for the utilisation of entomopathogenic nematodes as either inoculative or inundative agents for suppression of scarab larvae.
- Page 59Abstract
Studies during the last decade on using entomopathogenic nematodes to control Carposina niponensis, the most important pest of I million hectares of apple, pear and date, have indicated that nematodes could replace the currently used chemical insecticides. S. carpocapsae is best applied to the soil surface beneath apple trees during summer rains which stimulate Carposina larvae to emerge from the deep overwintering hibernacula and migrate to the surface to pupate. During this period, the larvae are most susceptible to nematodes and the soil ideal for nematode penetration. In field trials conducted in a variety of apple orchards in many provinces in China larval mortality ranged from 91.8%–98.4%; fruit damage indices and pheromone monitoring have indicated that control by S. carpocapsae is better than with insecticides. During this collaborative project, under the auspices of the Australian Centre for International Agricultural Research, scientists from the Cuangdong Entomological Institute, the Biological Control Institute, CAAS in Beijing and the Division of Entomology, CSIRO, Australia, are also working together to develop efficient mass production and processing of S. carpocapsae on a pilot factory scale and to coordinate field and grower trials over hundreds of hectares of orchards throughout apple growing regions in China.
- Page 67Abstract
Entomopathogenic nematodes can control insect pests in soil but to achieve control, large numbers of infective stage juveniles need to be inundatively released at rates of 105–106 per m2. Only a proportion (e.g. 20–30% for S. carpocapsa) of these released nematodes are able to invade and kill insects at any given time. Moreover, as little as 10% of the initial inoculum is present in the soil 7 days post-application. Abiotic and biotic components of the soil environment influence nematode infectivity and persistence. However, recent evidence suggests that intrinsic genetic, physiological and behavioural characteristics of the infective stage are also important. These intrinsic factors may be amenable to manipulation, with the possibility that correct choice of method for production, formulation, application technique as well as nematode species and strains can improve the infectivity and persistence of entomopathogenic nematodes in soil. Such improvements in infectivity and persistence may permit lower application rates and thus open up a broader range of insects to economic control. It is recommended that persistence in soil should be included in screening programs for efficacy of entomopathogenic nematodes.
- Page 79Abstract
Very little is known of the factors that affect the pathogenicity of infective dauer juveniles of entomopathogenic nematodes. It has been assumed that outside the host in the soil environment the physiological fitness of dauers, as measured by available food reserves, will play an important role in quiescent survival during host absence. No dauers have been able to survive cryptobiotically. However, all dauers released from the host may not be equally physiologically fit since there are different generations involved. We are also unaware as to whether quiescence and/or cryptobiosis are the only modes of dormancy during host absence or whether a diapause phenomenon exists. Preliminary observations infer the latter in some cases and suggest that not all dauers in a given population are capable of this response. As for cyst nematodes there may be a mixture of dormant conditions that allow slow release of dauers into the active state, but all may not be immediately pathogenic on revival. Ultimately, those factors involved with the correct development of the dauer within the host (i.e. host physiology/biochemistry, time of production) will affect the behaviour of the dauer outside the host and will have the greatest effect on pathogenicity. Thus, although the production of large numbers of dauers on exotic hosts or in culture poses no problems, the quality of the dauer produced, in terms of pathogenicity, may be different from that obtained using the natural host. In many cases natural hosts have still to be identified.
- Page 89Abstract
Expanded use of entomopathogenic nematodes in biological control cannot be expected unless field efficacy is increased. The current ‘efficacy gap’ between nematodes and chemical insecticides might be bridged by matching nematode species and strains against those insects they are best adapted to parasitise. This approach requires understanding the adaptive nature of entomopathogenic nematodes, particularly how they locate, identify, and assess potential hosts. No single species or strain, including the All strain of Steinernema carpocapsae, will be effective against all insect pests. S. carpocapsae will be most useful if the target insects are highly mobile at, or near, the soil surface, or if the host is highly susceptible to infection (e.g. black vine weevil). Genetic selection is a viable approach to improving efficacy but cannot be expected to overcome poor adaptation. Attention must also be given to protecting the genetic variability of new isolates, preventing the loss of alleles through laboratory adaptation. Finally, it is essential that prediction models be developed so that nematodes will be used only when and where they are likely to be effective.
- Page 97Abstract
One of the constraints in the use of entomopathogenic nematodes as biological control agents is their interaction with other soil microorganisms. Competition studies with two species of entomopathogenic nematodes, particularly a heterorhabditid and a steinernematid, indicate that incompatibilities exist within an insect host usually resulting in the death of both nematode species. Although these incompatibilities occur within a host, the coexistence of two nematode species with different attack strategies may be possible because of spatial and temporal separation of the species. Similarly, entomopathogenic nematodes and the entomopathogenic fungus Beauveria bassiana are antagonistic to one another within the same host. Yet, coexistence in the soil is likely because the nematodes are not attracted to fungus-infected insects. The combined application of both pathogens should provide better reduction of a susceptible pest than either pathogen alone. The milky disease bacterium, Bacillus popilliae, a pathogen of scarabaeid larvae, and a heterorhabditid nematode show compatibility. Thus, B. popilliae may be used as a stressing agent to make scarabaeid larvae more susceptible to heterorhabditid infection. Finally, nematode-parasitic fungi may be antagonistic to entomopathogenic nematodes. For example, the fungus Hirsutella rhossiliensis infects several species of entomopathogenic nematodes. However, its infectivity varies between nematode species and a less-susceptible nematode species may be more efficacious against an insect pest in soils infested with this fungus.
- Page 105Abstract
Combinations of chemical or biological agents with steinernematid nematodes can increase the nematodes’ efficacy against insect pests. In particular, field applications of Steinernema carpocapsae with a given chemical pesticide (oxamyl, fenithrothion, diazinon, acephate, or permethrin) yielded better results for control of soil and foliage insect pests than an application of either the nematode or pesticide alone. However, combinations of nematodes and chemical pesticides in laboratory experiments provided mostly negative results for the infectivity of nematodes against a host insect. Although the nematodes were active in the chemical solutions, these activated movements did not result in enhanced infection of a host. When the nematodes had a substrate which allowed them to nictate, the pesticides enhanced their nictating behaviour, resulting in a corresponding increase in insect mortality. In fumigated soil, the persistence of S. carpocapsae was not only prolonged but the recovery of plant-parasitic nematodes was suppressed. This longer persistence served as a prophylactic treatment against the invasion of soil insect pests. Finally, combining S. carpocapsae and the fungivorous nematode, Aphelenchus avenae, provided simultaneous control of a susceptible soil insect pest and a phytoparasitic fungus.
- Page 115Abstract
Temperature is an important factor limiting the success of field applications of steinernematid and heterorhabditid nematodes for the control of pest insects. Prospects for improved control at high and low temperatures are discussed. Strategies include the identification of pre-adapted wild types, selective breeding, and optimisation of pre-application conditions.
- Page 127Abstract
The usefulness of steinernematid and heterorhabditid nematodes for the control of insect pests depends entirely on their symbiotic associations with bacteria (Xenorhabdus spp.). The nematode functions as a vector transmitting its symbiotic bacterium into the host haemocoel and providing partial protection from the host’s immune defence response. The bacterium multiplies, producing toxins that kill the host and providing and protecting essential nutrition for the nematodes. The major elements of the nematode/bacterium/insect interactions are reviewed. Particular consideration is given to phase variation in the symbiotic bacteria, an important factor in the nematode/bacterium interaction and mass production.
- Page 137Abstract
Bacteriocins occur naturally in small quantities in the two phases of Xenorhabdus nematophilus A24 and F1, X. bovienii Dan, X. beddingii Q58 and X. luminescens K80. After induction by mitomycin C or by high temperature, bacteriocins and phages were detected in greater quantities in each of these cultures, except X. luminescens K80. These bacteriocins, produced by both phases, and the previously identified water-soluble antibiotics, produced only by phase 1, are important in establishing the monoxenic conditions observed during the parasitic development of the host nematode in insect cadavers. The significance of the Xenorhabdus lysogeny is discussed with related preliminary data and recent reports from other researchers.
- Page 147Abstract
The role of fimbriae in the specific retention of Xenorhabdus nematophilus within the intestine of infective juveniles of the entomopathogenic nematode Steinernema carpocapsae is under investigation. In this study we purified the fimbriae and raised antibodies against them. We then used antibody/gold labelling to show the specificity of the antibodies to localise Xenorhabdus fimbriae within the intestine of S. carpocapsae. The morphology of the fimbriae suggests that they may analogous to Type I of other En teroba cteria ceae.
- Page 164Abstract
Various insect pests are controlled by entomogenous and entomopathogenic nematodes and more progress will be made in the use and commercialisation of these nematodes as the knowledge already garnered is applied. However, the discipline of insect nematology must be developed further if the full potential of nematodes for insect control is to be realised. This chapter examines the possibilities for improving the prospects of nematodes as alternatives to chemical insecticides. It includes consideration of production, storage and application as well as those aspects of nematode ecology, physiology, genetics and bacteriology affecting insect control.
