In 1979, only a single strain of a single species of entomopathogenic nematode, the "All" strain of Steinernema carpocapsae, was commercially available. The hopes and dreams of this fragile infant industry, not to mention those of academic researchers, rested entirely on what proved to be a very narrow foundation. Today, 20 years after S. carpocapsae was first introduced, seven nematode species have been commercialized, six of which are still available, five in the U.S. What drove this expansion? Just as with chemical insecticides, consumers need different nematodes to match different pest biologies.
But in the beginning, the conventional thinking among many, especially in industry, was that S. carpocapsae was some sort of biological "silver bullet." And, indeed, this nematode was well known to be lethal to hundreds of diverse pest species, from termites to caterpillars, fleas to black widow spiders. This nematode seemed to have a host range not unlike the organophosphates and carbamates that then dominated the insecticide scene, and this, coupled with their exemption from government registration sparked keen interest from industry.
Yet when field tested against these same insects, the nematode worked sometimes but more often failed, usually miserably. The conventional wisdom began to grow that nematodes "don't work" when the only truth actually revealed was that nematodes don't work for that particular insect. Just as imidacloprid is a wonderful chemical agent against many white grub species but is nearly useless against carpenter ants, S. carpocapsae is effective against webworms but ineffective for mushroom flies yet S. feltiae is an excellent match against these flies.
The extraordinarily wide spectrum of activity attributed to S. carpocapsae is largely based on experimental infections. In lab exposures, conducted in petri plates, host-parasite contact is assured, host escape is impossible, and environmental conditions of temperature, moisture, and light are optimal for infection. In the field, behavioral and environmental barriers come into play and restrict host range. An experimental (i.e. lab-derived) host range should not be confused with field activity. Experimental host ranges can be huge. But in the real world there are barriers that can disrupt the infection process, frustrating control efforts and resulting in a far narrower spectrum of insecticidal activity. It is these barriers that require careful matching of nematode and insect.
Infection barriers are all part of the host selection process for entomopathogenic nematodes, which consists of four sequential steps: 1) host-habitat finding, 2) host-finding, 3) host acceptance, and 4) host suitability. Each step acts as a sort of biological sieve, narrowing an experimental to a field host range. If our goal as practitioners is to match target insects with the nematode species best able to parasitize it, we must understand and appreciate each step.
1) Host-Habitat Finding. This simply means that parasite and host must coincide in time and space. For example, mosquito and blackfly larvae are good experimental but poor field hosts because nematodes are not adapted to the aquatic environment and quickly settle out of the host-feeding zone. Cabbage loopers are easy for nematodes to kill in the lab but they can rarely tolerate the physical extremes characteristic of exposed foliage: rapid desiccation, high surface temperature, and exposure to solar radiation. Nematodes are soil adapted. The soil environment buffers them against extremes of the aboveground world. Overwhelmingly, nematodes are most effective when soil insects are the target pests.
Every rule has exceptions. As soil organisms, nematodes certainly did not evolve for life within stems; however, this is an example of a microhabitat that coincidentally offers the same shelter from environmental extremes as the soil. Thus nematodes injected into wood galleries and other cryptic habitats tend to perform their insect-killing role well. Such applications bypass the host habitat barrier. In addition, habitats can be modified to make them more favorable. Nematodes were effective against foliage-feeding caterpillars when commercial chrysanthemums were sheltered under shade-cloth, eliminating use of three conventional chemical insecticides. Although nematodes applied outside their natural reservoir, the soil, have no prospects for establishment and recycling (e.g. long-term control), they do have utility where a short-term knockout blow must be delivered.
2) Host-finding. Once in the proper habitat, infective-stage nematodes must locate insect hosts. Host-finding strategies can be divided into two broad categories: ambushing and cruising. Ambusher and cruiser strategies can be distinguished by their contrasting host search behaviors. Cruiser nematode species such as S. glaseri and Heterorhabditis bacteriophora tend to be highly mobile in searching comparatively large areas for hosts, whereas ambusher species tend to remain stationary. The key reason for this dichotomy in behavior is nictation. Ambushers nictate, that is they search by standing on their tail, elevating most of their bodies free in the air. This sit-and-wait approach to find hosts serves as a mechanism for host attachment. Ambushers are unable to detect hosts resting only a few millimeters away. By contrast, cruisers are unable to nictate but are highly responsive to host-released volatiles like carbon dioxide, which they use to orient toward insects. Ambushing is clearly a surface-adapted behavior, as it is not possible to nictate effectively within the soil. And, indeed, soil sampling reveals that ambush species tend to be found in the upper soil stratum especially near the soil surface litter and duff. Cruiser species are found distributed throughout the soil profile as would be predicted from their search behavior.
If ambushing is a stationary behavior that occurs at or near the soil surface, then it follows that ambusher nematodes are best adapted to parasitize highly mobile, surface-adapted hosts (e.g. cutworms, armyworms). How effective, for example, could S. carpocapsae or S. scapterisci be expected to be against white grubs when both parasites and hosts are relatively sedentary and inhabit different parts of the soil profile? If cruising is a mobile behavior that occurs below ground, then cruiser nematodes must be best adapted to parasitize sedentary, below ground hosts such as white grubs. Thus, understanding host-finding strategies increases our ability to make efficacy predictions, thereby optimizing host-parasite matches.
Again, there are exceptions to this generalization. Host finding is a continuum. Ambusher species such as S. carpocapsae and S. scapterisici form one end of the continuum and cruisers such as H. bacteriophora and S. glaseri form the opposite end. Other species, notably S. riobravis and S. feltiae, are intermediate, doing a bit of both ambushing and cruising. We do not yet know where most species of the more than 30 species of entomopathogenic nematodes fall on the continuum.
3) Host Acceptance. An entomopathogenic nematode can parasitize only a single host, so each infective nematode must carefully assess an insect before committing irreversibly. Nematodes must be able to recognize their hosts so they don't make an irreconcilable mistake and attack a host that's unsuitable. In short, if they don't recognize a host, they shouldn't attack under most conditions.
Entomopathogenic nematodes are able to discriminate among potential hosts. S. carpocapsae is highly responsive to caterpillars, moderately responsive to white grubs, and is unable to differentiate between millipedes and plastic. This correlates positively with the suitability of these insects as hosts, thereby providing an excellent measure of adaptation and an excellent means for making more accurate nematode-insect matches. Once a potential host has been contacted and recognized, the insect is not defenseless.
Consider white grubs. The spiracles are a key portal of entry of S. carpocapsae attacking caterpillars, but white grub spiracles are covered with sieve plates that preclude invasion via this route. The alternate penetration route for this nematode tends to be the gut; but whereas the highly susceptible wax moth has a thin, loose peritrophic membrane lining the gut, white grubs possess a thick, multi-layered protective membrane. Therefore only highly adapted nematodes such as S. glaseri are a good match against these insect pests.
4) Host Suitability. Once a host has been located, recognized, and penetrated, the nematode's attack still may not succeed if the insect is able to respond with an effective immune response. The immune response also provides us with clues for making the most appropriate host-parasite matches, since a strong immune response suggests a low level of adaptation. Thus, S. carpocapsae is a poor match for Japanese beetle larvae where encapsulation begins immediately and melanization is complete in a few hours. By contrast, S. glaseri invasion elicits a weak immune response that is quickly defeated by the nematode-released anti-immune proteins. This would indicate that the latter nematode is the best match for control purposes, a prediction borne out by extensive field testing. Consideration of host suitability provides another measure useful in avoiding incompatible matches.
Five entomopathogenic nematode species are currently commercially available in the U.S. Each species is a very different organism. The following brief synopsis on each species is intended to guide users in making predictions regarding field performance.
S. carpocapsae. The most studied, available, and versatile of all entomopathogenic nematodes. Important attributes include ease of mass production and ability to formulate in a partially desiccated state that can provide several months of room-temperature shelf life. Particularly effective against caterpillars, including various webworms, cutworms, armyworms, girdlers, and wood-borers. This species is a classic sit-and-wait or "ambush" forager, standing on its tail in an upright position near the soil surface and attaching to passing hosts. Consequently, S. carpocapsae tends to be most effective when applied against highly mobile surface-adapted insects. Highly responsive to carbon dioxide once a host has been contacted, the spiracles are a key portal of host entry. It is most effective at moderate temperatures ranging from 72 to 82°F.
S. feltiae. Attacks primarily fly larvae, including mushroom flies, fungus gnats, and crane flies. This nematode is unique in maintaining infectivity at low soil temperatures, even below 50°F. S. feltiae offers lower stability than other steinernematids.
S. glaseri. The largest entomopathogenic nematode at twice the length but eight times the volume of S. carpocapsae infective juveniles, S. glaseri attacks beetle larvae, particularly those of scarabs. This species is a cruise forager, neither nictating nor attaching well to passing hosts, but highly mobile and responsive to long-range host volatiles. Thus, this nematode is best adapted to parasitize hosts possessing low mobility and residing within the soil profile. Field trials, particularly in Japan, have demonstrated that S. glaseri can provide good control of several scarab species. Large size however reduces yield, making this species more expensive to produce than other species. A tendency to occasionally "lose" its bacterial symbiont is troublesome. Moreover, the highly active and robust infective juveniles are difficult to contain within formulations that rely on partial nematode dehydration (e.g. clay granules). Additional technological advances are needed before this nematode is likely to realize its full potential.
S. riobravis. This highly pathogenic species, isolated to date only from the Rio Grande Valley of Texas, possesses several novel features. Its effective host range runs across multiple insect orders, a versatility likely due in part to its ability to exploit aspects of both ambusher and cruiser means of finding hosts. Trials have demonstrated its effectiveness against corn earworms, citrus root weevils, pink bollworms, and mole crickets. This is a high temperature nematode, effective at killing insects at soil temperatures above 95°F. Persistence is excellent even under semi-arid conditions, a feature no doubt enhanced by the high lipid levels found in infective juveniles. Its small size provides high yields whether using in vivo or in vitro methods. Only formulation improvements that impart increased commercial stability are needed for this parasite to achieve its full potential.
H. bacteriophora. Among the most important entomopathogenic nematodes, it possesses considerable versatility, attacking caterpillar and beetle larvae among other insects. This cruiser species appears most useful against root weevils, particularly black vine weevil where it has provided consistently excellent results in containerized soil. A warm temperature nematode, H. bacteriophora shows reduced efficacy when soil temperature drops below 68°F. Poor stability has limited the usefulness of this interesting nematode: shelf-life is problematic and most infective juveniles persist only a few days following application.
H. megidis. Isolated in Ohio, researched and developed in Europe, and now sold in the U.S., this nematode is marketed primarily against black vine weevil. Field results have been highly favorable in containerized soil although its large size, characteristic heterorhabditid instability, and dearth of field efficacy data against other insect pests limit its utility at present.
THE NEED TO KNOW MORE
Additional nematodes species are the subject of vigorous research and development efforts and may be considered to be in the "pipeline." H. indicus is a small, efficiently produced nematode said to be effective against white grubs and certain root weevils. S. kushidai, a Japanese nematode, shows good efficacy against white grubs and has excellent stability and persistence potential, but mass production so far is problematic. H. marelatus is efficacious against root weevils and active at cool soil temperatures. S. scapterisci, once wielded against mole crickets may make a comeback. Other species are also being evaluated in one or more of the 80 entomopathogenic nematode laboratories located around the world. Moreover, new strains of currently commercialized strains are the subject of studies aimed at improved pathogenicity, stability, yields, and more.
Nematode end-users will need to know more as new strains and species come "on-line" and further technological advances are made. Tools are available to assist users in staying current and making optimal nematode-insect matches. The best place to find relevant new information is the SARE Entomopathogenic Nematode Website. Particularly useful here is a comprehensive bibliography of the research literature that permits quick accessing of all published papers, particularly field trials, for any target insect of interest. The site's Electronic Expert Panel is an alternative means of getting answers to questions by tapping into the site's stable of international nematode authorities. Be prepared, however, for instances of inconclusive data or no data for a particular nematode-insect combination. This is best seen as an opportunity for end-users to cut new ground by experimentation.
- Randy Gaugler, Rutgers University
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