Stabilisation of heat tolerance traits in Heterorhabditis bacteriophora through selective breeding and creation of inbred lines in liquid culture

Entomopathogenic nematodes (EPNs) suffer from trait deterioration, a potential problem when these antagonists are transferred into artificial environments for mass production. In order to improve beneficial traits of EPN genetic selection and hybridization has been successfully carried out. Should these selected strains deteriorate during serial culturing the efforts would be in vain. Inbreeding might offer a possibility to stabilize traits but can also result in inbreeding depression. This study attempted to increase heat tolerance of Heterorhabditis bacteriophora by selective breeding for seven cycles either with nematodes propagated in vivo in Galleria mellonella or with in vitro propagated nematodes which were exposed to heat stress in monoxenic liquid culture. After release of the selection pressure, the tolerance was monitored over 15 additional reproductive cycles to compare the stability of the trait. Virulence of the selected strains was assessed to check for negative tradeoff effects. Heat tolerance was successfully increased in vivo (from 39.03 to 40.85 °C) and in vitro (from 39 to 40 °C) propagated H. bacteriophora, but could only be maintained in populations which were serially reared in liquid culture. When H. bacteriophora is cultured in vivo, reproduction by cross fertilization is possible. In in vitro culture male and female cannot mate and reproduction is solely by self-fertilizing hermaphrodite resulting in homozygous inbred lines. Trait deterioration seems to be restricted to in vivo propagated H. bacteriophora, whereas monoxenic liquid cultures handling large numbers of inbred lines provided genetically stable and virulent nematode populations. Selection using liquid culture technology is thus superior over in vivo propagation to sustain beneficial traits in H. bacteriophora not only for selective breeding but also for mass production.     

Effect of insect cadaver desiccation and soil water potential during rehydration on entomopathogenic nematode (Rhabditida: Steinernematidae and Heterorhabditidae) production and virulence

We examined the influence of insect cadaver desiccation on the virulence and production of entomopathogenic nematodes (EPNs), common natural enemies of many soil-dwelling insects. EPNs are often used in biological control, and we investigated the feasibility of applying EPNs within desiccated insect cadavers. Desiccation studies were conducted using the factitious host, Galleria mellonella (Lepidoptera: Pyralidae, wax moth larvae) and three EPN species (Heterorhabditis bacteriophora ‘HB1’, Steinernema carpocapsae ‘All’, and Steinernema riobrave). Weights of individual insect cadavers were tracked daily during the desiccation process, and cohorts were placed into emergence traps when average mass losses reached 50%, 60%, and 70% levels. We tracked the proportion of insect cadavers producing infective juveniles (IJs), the number and virulence of IJs produced from desiccated insect cadavers, and the influence of soil water potentials on IJ production of desiccated insect cadavers. We observed apparent differences in the desiccation rate of the insect cadavers among the three species, as well as apparent differences among the three species in both the proportion of insect cadavers producing IJs and IJ production per insect cadaver. Exposure of desiccated insect cadavers to water potentials greater than −2.75 kPa stimulated IJ emergence. Among the nematode species examined, H. bacteriophora exhibited lower proportions of desiccated insect cadavers producing IJs than the other two species. Desiccation significantly reduced the number of IJs produced from insect cadavers. At the 60% mass loss level, however, desiccated insect cadavers from each of the three species successfully produced IJs when exposed to moist sand, suggesting that insect cadaver desiccation may be a useful approach for biological control of soil insect pests.     

Genetic improvement of the biological control nematode Heterorhabditis bacteriophora (Rhabditidomorpha: Heterorhabditidae): heterosis effect enhances desiccation but not heat tolerance

The entomopathogenic nematode Heterorhabditis bacteriophora is commercially used in biological control of soil dwelling insect pests. It reproduces by autogamy (hermaphrodites) enabling the production of inbred lines, but also by amphimixis (through mating of male and female) which allows cross-breeding. When H. bacteriophora is produced in liquid culture, copulation of male and female is prevented and reproduction is solely by self-fertilisation of hermaphrodites. When reared in insects, crosses are possible resulting in heterozygous offspring. Heat and desiccation tolerance of these nematodes have been successfully improved by selective breeding. Trait deterioration was prevented by producing homozygous inbreds through consecutive reproduction in liquid culture, the method also used for commercial mass production. In this study, we investigated possible heterosis effects in desiccation and heat tolerance after cross-breeding of homozygous inbred lines of H. bacteriophora. Increased desiccation tolerance of the heterozygous progeny in comparison to homozygous inbred lines was recorded indicating that heterosis is a possible means for further improvement of this trait. In contrast, the heat tolerance of the heterozygous offspring was lower than that of the homozygous population. The results provide evidence for the tremendous potential of classical genetics to improve beneficial traits of a biological control agent and carry domestication of H. bacteriophora a significant step forward.     

昆虫病原线虫的耐寒性

昆虫病原线虫可开发成生物农药,广泛应用于多种地下及钻蛀害虫的安全防治。但昆虫病原线虫货架期较短,对寒冷等极端环境的耐受性较差,影响了其在生物防治方面的商业开发。本文介绍了寒区的昆虫病原线虫资源,总结了昆虫病原线虫耐寒性的测定方法及增强方法、耐寒性差异的研究进展,并对其耐寒的生理生化机制及分子机理进行了综述。研究昆虫病原线虫的耐寒性,对于解释种群动态,指导昆虫病原线虫的低温保存,以及拓展其在生物防治方面的应用具有重要意义。     

Harmful effects of mustard bio-fumigants on entomopathogenic nematodes

Mustard (Brassica and Sinapis spp.) green manures tilled into the soil preceding potato crops act as bio-fumigants that are toxic to plant–parasitic nematodes, providing an alternative to synthetic soil fumigants. However, it is not known whether mustard green manures also kill beneficial entomopathogenic nematodes (EPNs) that contribute to the control of pest insects. We used sentinel insect prey (Galleria mellonella larvae) to measure EPN infectivity in Washington State (USA) potato fields that did or did not utilize mustard green manures. We found a trend toward lower rates of EPN infection in fields, where mustard green manures were applied, compared to those not receiving this cultural control method. In a series of bioassays we then tested whether the application of two mustard (Brassica juncea) cultivars, differing in glucosinolate levels, disrupted the abilities of a diverse group of EPN species to infect insect hosts. Mustard-exposure trials were conducted first in laboratory arenas where EPNs were exposed to mustard extracts suspended in water, and then in larger microcosms in the greenhouse where EPNs were exposed to green manure grown, chopped, and incorporated into field soil. In all trials we used G. mellonella larvae as hosts and included multiple EPN species in the genera Steinernema (Steinernema carpocapsae, Steinernema feltiae, Steinernema glaseri, and Steinernema riobrave) and Heterorhabditis (Heterorhabditis bacteriophora, Heterorhabditis marelatus, and Heterorhabditis megidis). In the laboratory, EPN infection rates were lower in arenas receiving mustard extracts than the control (water), and lower still when EPNs were exposed to extracts from plants with high versus low glucosinolate levels. Results were nearly identical when mustard foliage was soil-incorporated into greenhouse microcosms, except that the negative effects of mustards on EPNs developed more slowly in soil. Significantly, in arenas of both types one EPN species, S. feltiae, appeared to be relatively unaffected by mustard exposure. Together, our results suggest that the use of mustard bio-fumigants for the control of plant–parasitic nematodes has the potential to interfere with the biocontrol of insect pests using EPNs. Thus, it may be difficult to combine these two approaches in integrated pest management programs.     

Entomopathogenic Nematode Production and Application Technology

Production and application technology is critical for the success of entomopathogenic nematodes (EPNs) in biological control. Production approaches include in vivo, and in vitro methods (solid or liquid fermentation). For laboratory use and small scale field experiments, in vivo production of EPNs appears to be the appropriate method. In vivo production is also appropriate for niche markets and small growers where a lack of capital, scientific expertise or infrastructure cannot justify large investments into in vitro culture technology. In vitro technology is used when large scale production is needed at reasonable quality and cost. Infective juveniles of entomopathogenic nematodes are usually applied using various spray equipment and standard irrigation systems. Enhanced efficacy in EPN applications can be facilitated through improved delivery mechanisms (e.g., cadaver application) or optimization of spray equipment. Substantial progress has been made in recent years in developing EPN formulations, particularly for above ground applications, e.g., mixing EPNs with surfactants or polymers or with sprayable gels. Bait formulations and insect host cadavers can enhance EPN persistence and reduce the quantity of nematodes required per unit area. This review provides a summary and analysis of factors that affect production and application of EPNs and offers insights for their future in biological insect suppression.     

Genetics of the Nematode Heterorhabditis bacteriophora Strain HP88: The Diversity of Beneficial Traits

Genotypic variation among infective juveniles of Heterorhabditis bacteriophora (strain HP88) in heat, desiccation, ultraviolet tolerance, and host-finding ability was assessed by comparing the performance of inbred lines of this entomopathogenic nematode in laboratory assays. Each line consisted of highly homozygous offspring originating from one individual obtained from a natural population. Considerable variation in all four traits was detected among the different inbred lines. The heritability values for heat or ultraviolet tolerance and for host-finding ability were high, indicating that selection should be an efficient way for improving these traits in the population. The results for desiccation tolerance varied considerably within each line. Heritability value was low, indicating that the results were influenced mainly by environmental variation and suggesting that selective breeding for higher desiccation tolerance would be inefficient. Improvement through induction of mutations may be a better alternative in this population.     

A Realistic Appraisal of Methods to Enhance Desiccation Tolerance of Entomopathogenic Nematodes

Understanding the desiccation survival attributes of infective juveniles of entomopathogenic nematodes (EPN) of the genera Steinernema and Heterorhabditis, is central to evaluating the reality of enhancing the shelf-life and field persistence of commercial formulations. Early work on the structural and physiological aspects of desiccation survival focused on the role of the molted cuticle in controlling the rate of water loss and the importance of energy reserves, particularly neutral lipids. The accumulation of trehalose was also found to enhance desiccation survival. Isolation of natural populations that can survive harsh environments, such as deserts, indicated that some populations have enhanced abilities to survive desiccation. However, survival abilities of EPN are limited compared with those of some species of plant-parasitic nematodes inhabiting aerial parts of plants. Research on EPN stress tolerance has expanded on two main lines: i) to select strains of species, currently in use commercially, which have increased tolerance to environmental extremes; and ii) to utilize molecular information, including expressed sequence tags and genome sequence data, to determine the underlying genetic factors that control longevity and stress tolerance of EPN. However, given the inherent limitations of EPN survival ability, it is likely that improved formulation will be the major factor to enhance EPN longevity and, perhaps, increase the range of applications.     

Improvement of heat and desiccation tolerance in <Emphasis Type="Italic">Heterorhabditis bacteriophora</Emphasis> through cross-breeding of tolerant strains and successive genetic selection

Genetic selection can be a powerful tool to increase beneficial traits in biological control agents. In this study the heat and desiccation tolerance of the entomopathogenic nematode Heterorhabditis bacteriophora Poinar (Rhabditidomorpha: Strongyloidea) were significantly increased by cross breeding tolerant parental strains and successive genetic selection. These strains originated from a prior screening among 60 strains for increased stress tolerance. During genetic selection, the selection pressure was constantly increased and only the most tolerant 10% of the nematode populations were propagated for further selection steps. Assessment of tolerance and selection for both traits was performed with and without prior adaptation to the stress conditions. Eleven selection steps were performed to increase heat tolerance. A final overall increase in mean heat tolerance of 5.5°C was achieved when nematodes had been adapted to heat stress. For non-adapted tolerance an increase of 3.0°C from 40.1°C to 43.1°C was recorded. For comparison, a commercial strain had a mean tolerated temperature after adaptation of 38.2°C and of 36.5°C without adaptation. For assessment of the desiccation tolerance the mean tolerated water activity (a_w-value) of a population was measured. Cross-breeding most tolerant strains reduced the a_w-value from 0.67 to 0.65 after adaptation and from 0.9 to 0.7 without prior adaptation. The following six selection steps could not increase the tolerance whether nematodes had been adapted to stress or not. In comparison, the commercial strain tolerated a mean a_w-value of 0.985 after adaptation and 0.951 without adaptation. Further investigation will have to assess trait stability and possible trade-off effects. This study is a first important step on the road towards domestication of the entomopathogenic nematode H. bacteriophora.     

Viability and Virulence of Entomopathogenic Nematodes Exposed to Ultraviolet Radiation

Entomopathogenic nematodes (EPNs) can be highly effective biocontrol agents, but their efficacy can be reduced due to exposure to environmental stress such as from ultraviolet (UV) radiation. Our objectives were to 1) compare UV tolerance among a broad array of EPN species, and 2) investigate the relationship between reduced nematode viability (after exposure to UV) and virulence. Nematodes exposed to a UV radiation (254 nm) for 10 or 20 min were assessed separately for viability (survival) and virulence to Galleria mellonella. We compared 9 different EPN species and 15 strains: Heterorhabditis bacteriophora (Baine, fl11, Oswego, and Vs strains), H. floridensis (332), H. georgiana (Kesha), H. indica (HOM1), H. megidis (UK211), Steinernema carpocapsae (All, Cxrd, DD136, and Sal strains), S. feltiae (SN), S. rarum (17C&E), and S. riobrave (355). In viability assessments, steinernematids, particularly strains of S. carpocapsae, generally exhibited superior UV tolerance compared with the heterorhabditids. However, some heterorhabditids tended to be more tolerant than others, e.g., H. megidis and H. bacteriophora (Baine) were most susceptible and H. bacteriophora (Vs) was the only heterorhabditid that did not exhibit a significant effect after 10 min of exposure. All heterorhabditids experienced reduced viability after 20 min exposure though several S. carpocapsae strains did not. In total, after 10 or 20 min exposure, the viability of seven nematode strains did not differ from their non-UV exposed controls. In virulence assays, steinernematids (particularly S. carpocapsae strains) also tended to exhibit higher UV tolerance. However, in contrast to the viability measurements, all nematodes experienced a reduction in virulence relative to their controls. Correlation analysis revealed that viability among nematode strains is not necessarily related to virulence. In conclusion, our results indicate that the impact of UV varies substantially among EPNs, and viability alone is not a sufficient measure for potential impact on biocontrol efficacy as other characters such as virulence may be severely affected even when viability remains high.     

Long-Term Persistence of Yersinia pseudotuberculosis in Entomopathogenic Nematodes

Entomopathogenic nematodes (EPNs) are small worms whose ecological behaviour consists to invade, kill insects and feed on their cadavers thanks to a species-specific symbiotic bacterium belonging to any of the genera Xenorhabdus or Photorhabdus hosted in the gastro-intestinal tract of EPNs. The symbiont provides a number of biological functions that are essential for its EPN host including the production of entomotoxins, of enzymes able to degrade the insect constitutive macromolecules and of antimicrobial compounds able to prevent the growth of competitors in the insect cadaver. The question addressed in this study was to investigate whether a mammalian pathogen taxonomically related to Xenorhabdus was able to substitute for or “hijack” the symbiotic relationship associating Xenorhabdus and Steinernema EPNs. To deal with this question, a laboratory experimental model was developed consisting in Galleria mellonella insect larvae, Steinernema EPNs with or without their natural Xenorhabdus symbiont and Yersinia pseudotuberculosis brought artificially either in the gut of EPNs or in the haemocoel of the insect larva prior to infection. The developed model demonstrated the capacity of EPNs to act as an efficient reservoir ensuring exponential multiplication, maintenance and dissemination of Y. pseudotuberculosis.     

Natural enemies of natural enemies: the potential top‐down impact of predators on entomopathogenic nematode populations

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The effect of agitation system, temperature of the spray liquid, nematode concentration, and air injection on the viability of Heterorhabditis bacteriophora

Entomopathogenic nematodes (EPNs) are a group of potentially effective bio-insecticides to which Heterorhabditis bacteriophora, an active ingredient of several commercialised products, belongs. The application of the spray liquid with a motorised hydraulic sprayer introduces several stress factors to EPNs that may reduce their viability. Therefore, the effects of the agitation system, initial temperature of the spray liquid, EPN concentration, and additional air injection on the viability of EPNs were studied. The results clearly illustrate that the hydraulic agitation caused significantly more reduction in viability than the mechanical agitation. A lower temperature of the initial spray liquid, however, yielded a significantly higher EPN viability compared to a higher temperature after hydraulic mixing and so did air injection while EPN concentration did not significantly influence viability. Thus, the results clearly suggest that, with hydraulic agitation, both the re-circulation stress and the temperature increase significantly decreased the EPN viability, while air injection significantly improved it. Therefore, specific application conditions of living organisms in sprayer design and during application should be considered. Furthermore, spray water of less than 20°C should be used to keep temperature under control.     

Grower Acceptance of Entomopathogenic Nematodes: Case Studies on Three Continents

Projects to manage arthropod pests using entomopathogenic nematodes (EPNs) in Brazil, Korea and USA are reviewed to identify conditions and practices that affected the use of EPNs for pest management. A proliferation of covered agriculture in Korea, the growth in demand for high value, pesticide-free produce in Korea and Brazil, and the cost-effectiveness of EPNs created favorable conditions for the widespread adoption of EPN products in Brazilian guava orchards and Korean vegetable greenhouses. In Florida, EPNs imported from South America function successfully as classical biocontrol agents against invasive mole crickets attacking pasture and turf. However, the low value of pasture and the availability of cost-effective chemical insecticides in turf have depressed the demand for EPN products to control mole crickets. In Florida citrus orchards, a recent, dramatic increase in the use of chemical insecticides to control an arthropod vector of a devastating bacterial disease of citrus (huanglongbing) reduced the demand for EPN products to control Diaprepes root weevils. Nevertheless, a rich and diverse EPN fauna in the Florida peninsula provides significant control of subterranean stages of root weevils in some habitats, and is the focus of research to develop cultural practices that exploit the potential for increased pest management through EPN conservation.     

Screening Spanish isolates of steinernematid nematodes for use as biological control agents through laboratory and greenhouse microcosm studies

Entomopathogenic nematodes (EPNs) are one of the best non-chemical alternatives for insect pest control, with native EPN strains that are adapted to local conditions considered to be ideal candidates for regional biological control programs. Virulence screening of 17 native Mediterranean EPN strains was performed to select the most promising strain for regional insect pest control. Steinernema feltiae (Filipjev) (Rhabditida: Steinernematidae) Rioja strain produced 7%, 91% and 33% larval mortality for the insects Agriotes sordidus (Illiger) (Coleoptera: Elateridae), Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) and Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), respectively, and was selected as the most promising strain. The S. feltiae Rioja strain-S. littoralis combination was considered the most suitable to develop the Rioja strain as a biocontrol agent for soil applications. The effect of soil texture on the virulence of the Rioja strain against S. littoralis was determined through dose-response experiments. The estimated LC₉₀ to kill larvae in two days was 220, 753 and 4178 IJs/cm² for soils with a clay content of 5%, 14% and 24%, respectively, which indicates that heavy soils produced negative effects on the virulence of the Rioja strain. The nematode dose corresponding to the LC₉₀ for soils with a 5% and 14% clay content reduced insect damage to Capsicum annuum Linnaeus (Solanales: Solanaceae) plants under greenhouse microcosm conditions. The results of this research suggest that an accurate characterization of new EPN strains to select the most suitable combination of insect, nematode and soil texture might provide valuable data to obtain successful biological control under different ecological scenarios in future field applications.     

Genetic Variability in Stress Tolerance and Fitness among Natural Populations of Steinernema carpocapsae

Genetic variability in stress tolerance (heat, desiccation, and hypoxia) and fitness (virulence and reproduction potential) among natural populations of Steinernema carpocapsae was assessed by estimating phenotypic differences. Significant differences were observed in stress tolerance among populations. Populations isolated from North Carolina showed significantly more stress tolerance than those isolated from Ohio. Significant differences were also observed in populations isolated from the same locality. Survival of infective juveniles after exposure to 40°C for 2 h ranged from 37 to 82%. A threefold difference was observed in infective juvenile survival following exposure to osmotic desiccation or hypoxic condition. Several populations tested were superior to the most widely used strain (‘All’ strain) in stress tolerance traits, with one population KMD33, being superior to the ‘All’ strain in all traits. Fitness as expressed by virulence and reproductive potential differed significantly among populations but showed less variability than the stress tolerance traits. All populations tested had a reproductive potential greater than or similar to that of the ‘All’ strain and most of them caused >60% insect mortality of the wax moth larvae, Galleria mellonella. The high genetic variability in stress tolerance among natural populations suggests the feasibility of using selection for genetic improvement of these traits.     

Production of entomopathogenic nematodes in submerged monoxenic culture: A review

Monoxenic liquid culture is the most suitable technology for scaling up to industrial production of entomopathogenic nematodes (EPNs); however, the variability of the yield production remains a current problem in the process. The aim of this study was to analyze the parameters and criteria for EPN production in liquid culture based on scientific and technological knowledge from the last two decades. While experimental research has permitted the yield production of Heterorhabditis bacteriophora (362 × 10³ infective juveniles [IJs]/ml) and Steinernema carpocapsae (252 × 10³ IJs/ml), simultaneously, theoretical approaches have contributed to the understanding of the culture process, based on biological parameters of the bacterium–nematode complex and hydrodynamic and rheological parameters of the complex gas–liquid–solid system. Under this interdisciplinary research approach, bioprocess and biosystem engineering can contribute to design the various control strategies of the process variables, increase the productivity, and reduce the variability that until now distinguishes the in vitro production of EPNs by the liquid culture.     

Biocontrol potential of the entomopathogenic nematodes Heterorhabditis bacteriophora and Steinernema carpocapsae on cucurbit fly,Dacus ciliatus (Diptera: Tephritidae)

Entomopathogenic nematodes (EPNs) from the families Steinernematidae and Hererorhabditidae are considered excellent biological control agents against many insects that damage the roots of crops. In a regional survey, native EPNs were isolated, and laboratory and greenhouse experiments were conducted to determine the infectivity of EPNs against the cucurbit fly, Dacus ciliatus Loew (Diptera: Tephritidae). Preliminary experiments showed high virulence by a native strain of Heterorhabditis bacteriophora Poinar (Rhabditida: Heterorhabditidae) and a commercial strain of Steinernema carpocapsae Weiser (Rhabditida: Steinernematidae). These two strains were employed for further analysis while another native species, Steinernema feltiae, was excluded due to low virulence. In laboratory experiments, larvae and adult flies were susceptible to nematode infection, but both nematode species induced low mortality on pupae. S. carpocapsae had a significantly lower LC₅₀ value against larvae than H. bacteriophora in filter paper assays. Both species of EPNs were effective against adult flies but S. carpocapsae caused higher adult mortality. When EPN species were applied to naturally infested fruit (150 and 300 IJs/cm²), the mortality rates of D. ciliatus larvae were 28% for S. carpocapsae and 12% for H. bacteriophora. Both EPN strains successfully reproduced and emerged from larvae of D. ciliates. In a greenhouse experiment, H. bacteriophora and S. carpocapsae had similar effects on fly larvae. Higher rates of larval mortality were observed in sandy loam and sand soils than in clay loam. The efficacy of S. carpocapsae and H. bacteriophora was higher at 25 and 30°C than at 19°C. The results indicated that S. carpocapsae had the best potential as a biocontrol agent of D. ciliatus, based on its higher virulence and better ability to locate the fly larvae within infected fruits.     

Substrate modulation, group effects and the behavioral responses of entomopathogenic nematodes to nematophagous fungi

Laboratory experiments were conducted on the behavioral responses of five species of entomopathogenic nematodes (EPNs; Steinernema diaprepesi, Steinernema sp. glaseri-group, Steinernema riobrave, Heterorhabditis zealandica, Heterorhabditis indica) to three species of nematophagous fungi (NF; trapping fungus Arthrobotrys gephyropaga; endoparasites Myzocytium sp., Catenaria sp.). We hypothesized that EPN responses to NF and their putative semiochemicals might reflect the relative susceptibility of EPNs to particular NF species. EPN responses to “activated” NF (i.e., induced to form traps or sporangia by previous interactions with nematodes) versus controls of non-activated NF or heat-killed EPNs were compared in choice experiments on water agar in Petri dishes (dia = 9 cm) and in horizontal sand columns (8 cm L × 2.7 cm dia). On agar, all EPN species were attracted to all activated NF species except for S. riobrave, which was neutral. In sand, all EPN species were repelled by activated Arthrobotrys but attracted to activated Myzocytium and Catenaria, except H. indica (neutral to Myzocytium) and Steinernema sp. (neutral to Catenaria). EPN behavioral responses appeared unrelated to relative susceptibility to NF except that H. indica exhibited low susceptibility and a neutral response to Myzocytium in sand whereas the remaining EPNs were highly susceptible and attracted. These results indicate potential complexity (i.e., mixed responses, aggregation or group movement) and species specificity in the responses of EPNs to NF, demonstrate that results on agar can differ markedly from those in sand, and underline the potential importance of utilizing natural substrates to properly assess the role of semiochemicals in nematode-fungus interactions.     

The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes

Background

Entomopathogenic nematodes (EPNs) are tiny parasitic worms that parasitize insects, in which they reproduce. Their foraging behavior has been subject to numerous studies, most of which have proposed that, at short distances, EPNs use chemicals that are emitted directly from the host as host location cues. Carbon dioxide (CO₂) in particular has been implicated as an important cue. Recent evidence shows that at longer distances several EPNs take advantage of volatiles that are specifically emitted by roots in response to insect attack. Studies that have revealed these plant-mediated interactions among three trophic levels have been met with some disbelief.

Scope

This review aims to take away this skepticism by summarizing the evidence for a role of root volatiles as foraging cues for EPNs. To reinforce our argument, we conducted olfactometer assays in which we directly compared the attraction of an EPN species to CO₂ and two typical inducible root volatiles.

Conclusions

The combination of the ubiquitous gas and a more specific root volatile was found to be considerably more attractive than one of the two alone. Hence, future studies on EPN foraging behavior should take into account that CO₂ and plant volatiles may work in synergy as attractants for EPNs. Recent research efforts also reveal prospects of exploiting plant-produced signals to improve the biological control of insect pests in the rhizosphere.