Entomopathogenic nematode
Entomopathogenic nematodes are a group of nematodes, that cause death to insects. The term entomopathogenic has a Greek origin, with entomon, meaning insect, and pathogenic, which means causing disease. They are animals that occupy a biological control middle ground between microbial pathogens and predator/parasitoids. Although many other parasitic thread worms cause diseases in living organisms, entomopathogenic nematodes are specific in only infecting insects. Entomopathogenic nematodes live parasitically inside the infected insect host, and so they are termed as endoparasitic. They infect many different types of insects living in the soil like the larval forms of moths, butterflies, flies and beetles as well as adult forms of beetles, grasshoppers and crickets. EPNs have been found all over the world in a range of ecologically diverse habitats. They are highly diverse, complex and specialized. The most commonly studied entomopathogenic nematodes are those that can be used in the biological control of harmful insects, the members of Steinernematidae and Heterorhabditidae. They are the only insect-parasitic nematodes possessing an optimal balance of biological control attributes.
Classification
Life cycle
Because of their economic importance, the life cycles of the genera belonging to families Heterorhabditidae and Steinernematidae are well studied. Although not closely related, phylogenetically, both share similar life histories. The cycle begins with an infective juvenile, whose only function is to seek out and infect new hosts. When a host has been located, the nematodes penetrate into the insect body cavity, usually via natural body openings or areas of thin cuticle. After entering an insect, infective juveniles release an associated mutualistic bacterium from their gut which multiplies rapidly. These bacteria of the genus Xenorhabdus or Photorhabdus, for steinerernematides and heterorhabditids, respectively—cause host mortality within 24–48 hours. The nematodes provide shelter to the bacteria, which, in return, kill the insect host and provide nutrients to the nematode. Without this mutualism no nematode is able to act as an entomoparasite. Together, the nematodes and bacteria feed on the liquefying host, and reproduce for several generations inside the cadaver maturing through the growth stages of J2-J4 into adults. Steinernematids infective juveniles may become males or females, whereas heterorhabditids develop into self-fertilizing hermaphrodites with later generations producing two sexes. When food resources in the host become scarce, the adults produce new infective juveniles adapted to withstand the outside environment. The life cycles of the EPNs are completed within a few days. After about a week, hundreds of thousands of infective juveniles emerge and leave in search of new hosts, carrying with them an inoculation of mutualistic bacteria, received from the internal host environment. Their growth and reproduction depends upon conditions established in the host cadaver by the bacterium. The nematodes bacterium contributes anti-immune proteins to assist in overcoming their host defenses.Foraging strategies
The foraging strategies of entomopathogenic nematodes vary between species, influencing their soil depth distributions and host preferences. Infective juveniles use strategies to find hosts that vary from ambush and cruise foraging. In order to ambush prey, some Steinernema species nictate, or raise their bodies off the soil surface so they are better poised to attach to passing insects, which are much larger in size. Many Steinernema are able to jump by forming a loop with their bodies that creates stored energy which, when released, propels them through the air. Recent research has shown that this jumping behavior in Steinernema involves a reversible kink instability mechanism. By forming a closed loop and rapidly releasing stored elastic energy, nematodes such as Steinernema carpocapsae can achieve jumps up to 20 times their body length, enhancing their ability to disperse across complex terrains during host seeking.Other species adopt a cruising strategy and rarely nictate. Instead, they roam through the soil searching for potential hosts. These foraging strategies influence which hosts the nematodes infect. For example, ambush predators such as Steinernema carpocapsae infect more insects on the surface, while cruising predators like Heterorhabditis bacteriophora infect insects that live deep in the soil.
Population ecology
Competition and coexistence
Inside their insect hosts, EPNs experience both intra and interspecific competition. Intraspecific competition takes place among nematodes of the same species when the number of infective juveniles penetrating a host exceeds the amount of resources available. Interspecific competition occurs when different species compete for resources. In both cases, the individual nematodes compete with each other indirectly by consuming the same resource, which reduces their fitness and may result in the local extinction of one species inside the host. Interference competition, in which species compete directly, can also occur. For example, a steinernematid species that infects a host first usually excludes a heterorhabditid species. The mechanism for this superiority may be antibiotics produced by Xenorhabdus, the symbiotic bacterium of the steinernematid. These antibiotics prevent the symbiotic bacterium of the heterorhabditid from multiplying. In order to avoid competition, some species of infective juveniles are able to judge the quality of a host before penetration. The infective juveniles of S. carpocapsae are repelled by 24-hour-old infections, likely by the smell of their own species' mutualistic bacteria.Interspecific competition between nematode species can also occur in the soil environment outside of hosts. Millar and Barbercheck showed that the introduced nematode Steinernema riobrave survived and persisted in the environment for up to a year after its release. S. riobrave significantly depressed detection of the endemic nematode H. bacteriophora, but never completely displaced it, even after two years of continued introductions. S. riobrave had no effect on populations of the native nematode, S. carpocapsae, though, which suggests that coexistence is possible. Niche differentiation appears to limit competition between nematodes. Different foraging strategies allow two species to co-exist in the same habitat. Different foraging strategies separate the nematodes in space and enable them to infect different hosts. EPNs also occur in patchy distributions, which may limit their interactions and further support coexistence.
Population distribution
Entomopathogenic nematodes are typically found in patchy distributions, which vary in space and time, although the degree of patchiness varies between species. Factors responsible for this aggregated distribution may include behavior, as well as the spatial and temporal variability of the nematodes natural enemies, like nematode trapping fungus. Nematodes also have limited dispersal ability. Many infective juveniles are produced from a single host which could also produce aggregates. Patchy EPN distributions may also reflect the uneven distribution of host and nutrients in the soil. EPNs may persist as metapopulations, in which local population fragments are highly vulnerable to extinction, and fluctuate asynchronously. The metapopulation as a whole can persist as long as the rate of colonization is greater or equal to the rate of population extinction. The founding of new populations and movement between patches may depend on the movement of infective juveniles or the movement of infected hosts. Recent studies suggest that EPNs may also use non-host animals, such as isopods and earthworms for transport or can be scavengers.Community ecology
Parasites can significantly affect their hosts, as well as the structure of the communities to which they and their hosts belong. Entomopathogenic nematodes have the potential to shape the populations of plants and host insects, as well as the species composition of the surrounding animal soil community.Entomopathogenic nematodes affect populations of their insect hosts by killing and consuming individuals. When more EPNs are added to a field environment, typically at concentrations of, the population of host insects measurably decreases. Agriculture exploits this finding, and the inundative release of EPNs can effectively control populations of soil insect pests in citrus, cranberries, turfgrass, and tree fruit.
If entomopathogenic nematodes suppress the population of insect root herbivores, they indirectly benefit plants by freeing them from grazing pressure. This is an example of a trophic cascade in which consumers at the top of the food web exert an influence on the abundance of resources at the bottom. The idea that plants can benefit from the application of their herbivore's enemies is the principle behind biological control. Consequently, much of EPN biological research is driven by agricultural applications.
Examples of the top-down effects of entomopathogenic nematodes are not restricted to agricultural systems. Researchers at the Bodega Marine Laboratory examined the strong top-down effects that naturally occurring EPNs can have on their ecosystem. In a coastal shrubland food chain the native EPN, Heterorhabditis heplialus, parasitized ghost moth caterpillars, and ghost moth caterpillars consumed the roots of bush lupine. The presence H. heplialus correlated with lower caterpillar numbers and healthier plants. In addition, the researchers observed high mortality of bush lupine in the absence of EPNs. Old aerial photographs over the past 40 years indicated that the stands where nematodes were prevalent had little or no mass die-off of lupine. In stands with low nematode prevalence, however, the photos showed repeated lupine die-offs. These results implied that the nematode, as a natural enemy of the ghost moth caterpillar, protected the plant from damage. The authors even suggested that the interaction was strong enough to affect the population dynamics of bush lupine.
Not only do entomopathogenic nematodes affect their host insects, they can also change the species composition of the soil community. Many familiar animals like earthworms and insect grubs live in the soil, but smaller invertebrates such as mites, collembolans, and nematodes are also common. Aside from EPNs, the soil ecosystem includes predatory, bacteriovorous, fungivorous and plant parasitic nematode species. Since EPNs are applied in agricultural systems at a rate of, the potential for unintended consequences on the soil ecosystem appears large. EPNs have not had an adverse effect on mite and collembolan populations, yet there is strong evidence that they affect the species diversity of other nematodes. In a golf course ecosystem, the application of H. bacteriophora, an introduced nematode, significantly reduced the abundance, species richness, maturity, and diversity of the nematode community. EPNs had no effect on free-living nematodes. However, there was a reduction in the number of genera and abundance of plant-parasitic nematodes, which often remain enclosed within growths on the plant root. The mechanism by which insect parasitic nematodes have an effect on plant parasitic nematodes remains unknown. Although this effect is considered beneficial for agricultural systems where plant parasitic nematodes cause crop damage, it raises the question of what other effects are possible. Future research on the impacts EPNs have on soil communities will lead to greater understanding of these interactions.
In aboveground communities, EPNs have few side effects on other animals. One study reported that Steinernema felidae and Heterorhabditis megidis, when applied in a range of agricultural and natural habitats, had little impact on non-pest arthropods. Some minimal impacts did occur, however, on non-pest species of beetles and flies. Unlike chemical pesticides, EPNs are considered safe for humans and other vertebrates.