Entomopathogenic nematode
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Entomopathogenic nematodes (EPN) are a group of
nematodes The nematodes ( or grc-gre, Νηματώδη; la, Nematoda) or roundworms constitute the phylum Nematoda (also called Nemathelminthes), with plant-parasitic nematodes also known as eelworms. They are a diverse animal phylum inhabiting a broa ...
(thread worms), that cause death to insects. The term ''entomopathogenic'' has a Greek origin, with ''entomon'', meaning ''
insect Insects (from Latin ') are pancrustacean hexapod invertebrates of the class Insecta. They are the largest group within the arthropod phylum. Insects have a chitinous exoskeleton, a three-part body ( head, thorax and abdomen), three ...
'', and '' pathogenic'', which means ''causing disease''. They are
animals Animals are multicellular, eukaryotic organisms in the biological kingdom Animalia. With few exceptions, animals consume organic material, breathe oxygen, are able to move, can reproduce sexually, and go through an ontogenetic stage in ...
that occupy a bio control middle ground between microbial pathogens and
predator Predation is a biological interaction where one organism, the predator, kills and eats another organism, its prey. It is one of a family of common feeding behaviours that includes parasitism and micropredation (which usually do not kill th ...
/
parasitoids In evolutionary ecology, a parasitoid is an organism that lives in close association with its host at the host's expense, eventually resulting in the death of the host. Parasitoidism is one of six major evolutionary strategies within parasi ...
, and are habitually grouped with
pathogens In biology, a pathogen ( el, πάθος, "suffering", "passion" and , "producer of") in the oldest and broadest sense, is any organism or agent that can produce disease. A pathogen may also be referred to as an infectious agent, or simply a ger ...
, most likely because of their symbiotic relationship with
bacteria Bacteria (; singular: bacterium) are ubiquitous, mostly free-living organisms often consisting of one Cell (biology), biological cell. They constitute a large domain (biology), domain of prokaryotic microorganisms. Typically a few micrometr ...
. Although many other
parasitic Parasitism is a close relationship between species, where one organism, the parasite, lives on or inside another organism, the host, causing it some harm, and is adapted structurally to this way of life. The entomologist E. O. Wilson ha ...
thread worms cause diseases in living organisms (sterilizing or otherwise debilitating their host), entomopathogenic nematodes, are specific in only infecting insects. Entomopathogenic nematodes (EPNs) live parasitically inside the infected insect Host (biology), 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 in all over the world and 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 pest control, biological control of harmful insects, the members of Steinernematidae and Heterorhabditidae (Gaugler 2006). They are the only insect-parasitic nematodes possessing an optimal balance of biological control attributes. (Cranshaw & Zimmerman 2013).


Classification


Life cycle

Because of their economic importance, the Biological life cycle, life cycles of the genera belonging to families Heterorhabditidae and Steinernematidae are well studied. Although not closely related, phylogenetically, both share similar life histories (Poinar 1993). 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 (mouth, anus, spiracles) or areas of thin cuticle. (Shapiro-Ilan, David I., and Randy Gaugler. "Nematodes.") 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 (biology), 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.(Shapiro-Ilan, David I., and Randy Gaugler. "Nematodes.") 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 (Boemare 2002, Gaugler 2006). 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.(Shapiro-Ilan, David I., and Randy Gaugler. "Nematodes.")


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 (Campbell 1997). 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 (Campbell and Gaugler 1993). 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 (Campbell and Kaya 2000). 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 (Campbell and Gaugler 1993).


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 (Koppenhofer and Kaya 1996). 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 (Kaya and Koppenhofer1996). 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 ''Steinernema carpocapsae, S. carpocapsae'' are repelled by 24-hour-old infections, likely by the smell of their own species' mutualistic bacteria (Grewal ''et al.'' 1997). Interspecific competition between nematode species can also occur in the soil environment outside of hosts. Millar and Barbercheck (2001) 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 (ecology), 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 wiktionary:native, 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 (Kaya and Koppenhofer 1996).


Population distribution

Entomopathogenic nematodes are typically found in patchy distributions, which vary in space and time, although the degree of patchiness varies between species (reviewed in Lewis 2002). 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 (Lewis ''et al.'' 1998; Stuart and Gaugler 1994; Campbell ''et al.'' 1997, 1998). EPNs may persist as metapopulations, in which local population fragments are highly vulnerable to extinction, and fluctuate asynchronously (Lewis ''et al.'' 1998). The metapopulation as a whole can persist as long as the rate of colonization is greater or equal to the rate of population extinction (Lewis ''et al.'' 1998). The founding of new populations and movement between patches may depend on the movement of infective juveniles or the movement of infected hosts (Lewis ''et al.'' 1998). Recent studies suggest that EPNs may also use non-host animals, such as isopods and earthworms for transport (Eng ''et al.''2005, Shapiro ''et al.'' 1993) or can be scavengers (San-Blas and Gowen, 2008).


Community ecology

Parasites can significantly affect their hosts, as well as the structure of the biocoenosis, communities to which they and their hosts belong (Minchella and Scott 1991). 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 (Campbell et al. 1998, Strong et al. 1996). 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 (Lewis ''et al.'' 1998). 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 (nematodes) exert an influence on the abundance of resources (plants) 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 (Strong ''et al.'' 1996). 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 (Strong ''et al.'' 1996). 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 (Georgis et al. 1991), 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 (Somaseker ''et al.'' 2002). 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 (Bathon 1996). Unlike chemical pesticides, EPNs are considered safe for humans and other vertebrates.


Disturbance

Frequent disturbance often perturbs agricultural habitats and the response to disturbance varies among EPN species. In traditional agricultural systems, tilling disturbs the soil ecosystem, affecting biotic and abiotic factors. For example, tilled soils have lower microbial, arthropod, and nematode species diversity (Lupwayi ''et al.'' 1998). Tilled soil also has less moisture and higher temperatures. In a study examining the tolerances of different EPN species to tillage, the density of a native nematode, ''H. bacteriophora'', was unaffected by tillage, while the density of an introduced nematode, ''S. carpocapsae'', decreased. The density of a third nematode introduced to the system, ''Steinernema riobrave'', increased with tillage (Millar and Barbercheck 2002). Habitat preferences in temperature and soil depth can partially explain the nematodes' different responses to disturbance. ''S. carpocapsae'' prefers to remain near the soil surface and so is more vulnerable to soil disturbance than ''H. bacteriophora'', which forages deeper and can escape the effects of tillage. ''S. riobrave'' may have responded well to tillage because it is better at surviving and persisting in hotter and drier conditions created by tillage (Millar and Barbercheck 2002). The data showed that ''Steinernema'' sp. found in some Indonesia regions showed high adaptive capability when applied on another region or condition (Anton Muhibuddin, 2008). The response of EPNs to other forms of disturbance is less well defined. Nematodes are not affected by certain pesticides and are able to survive flooding. The effects of natural disturbances such as fire have not been examined.


Applications

Although the biological control industry has acknowledged EPNs since the 1980s, relatively little is understood about their biology in natural and managed ecosystems (Georgis 2002). Nematode-host interactions are poorly understood, and more than half of the natural hosts for recognized ''Steinernema'' and ''Heterorhabditis'' species remain unknown (Akhurst and Smith 2002). Information is lacking because isolates of naturally infected hosts are rare, so native nematodes are often baited using ''Galleria mellonella'', a lepidopteran that is highly susceptible to parasitic infection. Laboratory studies showing wide host ranges for EPNs were often overestimates, because in a laboratory, contact with a host is assured and environmental conditions are ideal; there are no "ecological barriers" to infection (Kaya and Gaugler 1993, Gaugler ''et al.'' 1997). Therefore, the broad host range initially predicted by assay results has not always translated into insecticidal success. Nematodes are open to mass production and don't require specialized application equipment since they are compatible with standard agrochemical equipment, including various sprayers (i.e. backpack, pressurized, mist, electrostatic, fan and aerial) and irrigation systems.(Cranshaw, & Zimmerman 2013). The lack of knowledge about nematode ecology has resulted in unanticipated failures to control pests in the field. For example, parasitic nematodes were found to be completely ineffective against blackflies and mosquitoes due to their inability to swim (Lewis ''et al.''1998). Efforts to control foliage-feeding pests with EPNs were equally unsuccessful, because nematodes are highly sensitive to UV light and desiccation (Lewis ''et al.''1998). Comparing the life histories of nematodes and target pests can often explain such failures (Gaugler ''et al.'' 1997). Each nematode species has a unique array of characteristics, including different environmental tolerances, dispersal tendencies, and foraging behaviors (Lewis ''et al.'' 1998). Increased knowledge about the factors that influence EPN populations and the impacts they have in their communities will likely increase their efficacy as biological control agents. Recently, studies have shown utilizing both EPNs (steinernematids and heterorhabditids) in combination for biological control of plum curculio in orchards in Northeast America have reduced populations by as much as 70-90% in the field, depending on insect stage, treatment timing and field conditions. More studies are being conducted for the efficacy of EPNs utilized as a biological control agent for organic growers as an alternative solution to chemistries that aren't as effective at controlling insect infestations.(Agnello, Jentsch, Shield, Testa, and Keller 2014).


See also

*Biological insecticides *Entomopathogenic fungus


References

*Akhurst R and K Smith 2002. "Regulation and safety". p 311–332 in Gaugler I, editor. ''Entomopathogenic Nematology''. CABI Publishing. New Jersey. *Boemare, N. 2002. "Biology, Taxonomy, and Systematics of Photorabdus and Xenorhabdus". p 57–78 in Gaugler I, editor. ''Entomopathogenic Nematology''. CABI Publishing. New Jersey. *Bathon, H. 1996. "Impact of entomopathogenic nematodes on non-target hosts". ''Biocontrol Science and Technology'' 6: 421–434. *Campbell, J.F. and R. Gaugler. 1993. "Nictation behavior and its ecological implications in the host search strategies of enomopathogenic nematodes". ''Behavior''. 126:155-169 Part 3-4 *Campbell, J.F. and Gaugler, R.R. 1997. "Inter-specific variation in entomopathogenic nematode foraging strategy: Dichotomy or variation along a continuum?" ''Fundamental and Applied Nematology'' 20 (4): 393–398. *Campbell JF; Orza G; Yoder F, Lewis E and Gaugler R. 1998. "Spatial and temporal distribution of endemic and released entomopathogenic nematode populations in turfgrass". ''Entomologia Experimentalis et Applicata''. 86:1-11. *Campbell J.F., and H.K. Kaya. 2000. "Influence of insect associated cues on the jumping behavior of entomopathogenic nematodes (Steinernema spp.)". ''Behavior'' 137: 591-609 Part 5. *Eng, M. S., E.L. Preisser, and D.R. Strong. 2005. "Phoresy of the entomopathogenic nematode Heterorhabditis marelatus by a non-host organism, the isopod Porcellio scaber". ''Journal of Invertebrate Pathology'' 88(2):173-176 *Gaugler. 1-2-06,
Nematodes-Biological Control
, editor-Contact Yaxin Li, Cornell University. *Gaugler R, Lewis E, and RJ Stuart. 1997. "Ecology in the service of biological control: the case of entomopathogenic nematodes". ''Oecologia''. 109:483-489. *Georgis R., H.K. Kaya, and R. Gaugler. 1991. "Effect of Steinernematid and Heterorhabditid nematodes (Rhabditida, Steinternematidae and Heterorhabditidae) on Nontarget Arthropods". ''Environmental Entomology''. 20(3): 815–822. *Georgis, R. 2002. "The Biosys Experiment: an Insider's Perspective". p 357–371 in Gaugler I, editor. ''Entomopathogenic Nematology''. CABI Publishing. New Jersey. *Grewal P.S., E.E. Lewis and R.Gaugler. 1997. "Response of infective stage parasites (Nematoda: Steinernematidae) to volatile cues from infected hosts". ''Journal of Chemical Ecology''. 23(2): 503–515. *Koppenhofer AM, and H.K. Kaya. 1996. "Coexistence of two steinernematid nematode species (Rhabditida: Steinernematidae) in the presence of two host species". ''Applied Soil Ecology''. 4(3): 221–230. *Kaya H.K., and A.M. Koppenhofer. 1996. "Effects of microbial and other antagonistic organism and competition on entomopathogenic nematodes". ''Biocontrol Science and Technology''. 6(3): 357–371. * *Lewis EE, Campbell JF and R Gaugler. 1998. "A conservation approach to using entomopathogenic nematodes in turf and landscapes". p 235–254 in P Barbosa Editor. ''Conservation Biological Control''. Academic Press. San Diego. *Lewis EE. 2002. Behavioural Ecology. p 205–224 in Gaugler I, editor. ''Entomopathogenic Nematology''. CABI Publishing. New Jersey. *Lupwayi, N.Z., W.A. Rice, and G.W. Clayton. 1998. "Soil microbial diversity and community structure under wheat as influenced by tillage and crop rotation". ''Soil Biological Biochemistry''. 30: 1733–1741. *Millar LC and ME Barbercheck. 2001. "Interaction between endemic and introduced entomopathogenic nematodes in conventional-till and no-till corn". ''Biological Control''. 22: 235–245. *Millar LC and ME Barbercheck.2002. "Effects of tillage practices on entomopathogenic nematodes in a corn agroecosystem". ''Biological control'' 25: 1–11. *Minchella, D.J. and M.E. Scott. 1991. "Parasitism-A cryptic determinant of animal community structure". ''Trends in Ecology and Evolution'' 6(8): 250–254. *Muhibuddin,A. 2008."Some Important Entomopathogenic Agens on Indonesia Region".''Irtizaq Press-Surabaya, Indonesia''. *Poinar, GO. 1993. "Origins and phylogenetic relationships of the entomophilic rhabditis, Heterorhabditis and Steinernema". ''Fundamental and Applied Nematology'' 16(4): 333–338. *San-Blas, E. and S.R. Gowen. 2008. "Facultative scavenging as a survival strategy of entomopathogenic nematodes". ''International Journal for Parasitology'' 38:85-91. *Shapiro, D.I.; Berry, E. C.; Lewis, L. C. 1993. "Interactions between nematodes and earthworms: Enhanced dispersal of Steinernema carpocapsae". ''Journal of Nematology'' 25(2): 189–192. *Somasekar N, Grewal PS, De Nardo EAB, and BR Stinner. 2002. "Non-target effects of entomopathogenic nematodes on the soil community". ''Journal of Applied Ecology''. 39: 735–744. *Stuart RJ and R Gaugler. 1994. "Patchiness in populations of entomopathogenic nematodes". ''Journal of Invertebrate Pathology''. 64: 39–45. *Strong, D. R., H.K. Kaya, A.V. Whipple, A.L, Child, S. Kraig, M. Bondonno, K. Dyer, and J.L. Maron. 1996. "Entomopathogenic nematodes: natural enemies of root-feeding caterpillars on bush lupine". ''Oecologia'' (Berlin) 108(1): 167–173. *Agnello, Art, Peter Jentsch, Elson Shield, Tony Testa, and Melissa Keller. "Evaluation of Persistent Entomopathogenic Nematodes." Evaluation of Persistent Entomopathogenic Nematodes for Biological Control of Plum Curculio 22.1 (Spring 2014): 21–23. Cornell University Dept. of Entomology. Web. *Cranshaw, W.S., and R. Zimmerman. "Insect Parasitic Nematodes." Insect Parasitic Nematodes. Colorado State University Extension, June 2013. Web. 3 July 2015.


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* [(https://bb.its.iastate.edu/bbcswebdav/pid-2172361-dt-content-rid-24641608_1/courses/12015-PL_P_-574_-XW/Lecture%204-2015.pdf{{dead link, date=January 2018 , bot=InternetArchiveBot , fix-attempted=yes ] Parasitic nematodes of animals Biological control agents of pest insects Soil biology