Phasmarhabditis hermaphrodita

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Phasmarhabditis hermaphrodita
Third stage Phasmarhabditis hermaphrodita.png
Third stage dauer larva

P. hermaphrodita

Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Nematoda
Class: Chromadorea
Order: Rhabditida
Family: Rhabditidae
Genus: Phasmarhabditis
Species:
P. hermaphrodita
Binomial name
Phasmarhabditis hermaphrodita
(A. Schneider, 1859)

Phasmarhabditis hermaphrodita is a facultative parasitic nematode that can kill slugs and snails. [1] It belongs to the family Rhabditidae, [1] the same family as Caenorhabditis elegans .

Contents

P. hermaphrodita is a bacterial-feeding nematode and is a lethal parasite of several terrestrial gastropod families such as Arionidae , Milacidae and Limacidae . [1] [2] It is also able to reproduce on rotting matter or penetrate and remain in resistant slug and snail species where it awaits for their death and will then reproduce on the cadaver (necromeny). P. hermaphrodita was first isolated and documented by A. Schneider in 1859 [1] [2] and was intensively studied in the 1990s by researchers at Long Ashton Research centre who were focused on finding a new biocontrol agent for slugs. P. hermaphrodita was isolated here and developed as a biological control agent (Nemaslug®) [3] [2] [4] for minimising agriculture damage from slugs and snails in 1994.

Anatomy

10x magnification photo of Adult Hermaphroditic Female nematode (Phasmarhabditis hermaphrodita). 1 Eye Piece Unit = 9.5mm 10x Magnification Anatomy scale of Female Phasmarhabditis hermaphrodita.jpg
10x magnification photo of Adult Hermaphroditic Female nematode (Phasmarhabditis hermaphrodita). 1 Eye Piece Unit = 9.5μm

P. hermaphrodita is unsegmented, vermiform, bilateral symmetrical pseudocoelomate. The body dimensions and structure of P. hermaphrodita is comparable to C. elegans' with a body length 1.3 - 1.7mm long [5] and an estimated circumference of 0.180mm. The primary structures are the Rhabditida-specific mouth, the pharynx, the intestine, the reproductive system (uterus, spermatheca, gonads) and the cuticle. Like all nematodes, it has four muscle bands that span the length of the body and has no devoted respiratory or circulatory system. [6] P. hermaphrodita has four larval stages before becoming a fully reproductive hermaphroditic adult female. [7] Males do exist in this species, but are very rare with Maupas only able to find 21 males among 15,000 individuals (0.14% of the population). [8] Third-stage dauer larvae are produced in unfavourable conditions such as low food levels, high population density or high temperatures. [9] Dauer larvae have constricted pharynx, double the thickness of a normal cuticle and increase of lipid droplets in their cytoplasm. [10] However, the most important aspect of the dauer stage is its ability to serve as the infective stage that seeks out new hosts, once the previous bacterial food source has been depleted. [11] [12] Dauers do not require a food source and can survive up to eight times longer than the original life span of a non-dauer nematode. [9] P. hermaphrodita is morphologically identical to two other Phasmarhabditis species P. neopapillosa [13] and P. tawfiki. [14] However, P. neopapillosa is a gonochoristic species with an equal number of males and females. [13]

Biological control of slugs

Terrestrial gastropods are a common problem in agricultural areas with a moist climate around the world, [15] crop damage occurs via the eating of leaves and stems and/or contaminating them with slime and faeces. [16] In the UK alone, slugs affect 59% of total area for rapeseed oil crops and 22% of wheat crops. [17] Without any type slug control for both rapeseed oil and wheat crops, the cost to the UK agricultural industry would be an approximate £43.5 million per year. [17]

Slug pest Deroceras reticulatum is a common agricultural and horticultural pest and is one of the host species affected by Phasmarhabditis hermaphrodita Deroceras reticulatum.png
Slug pest Deroceras reticulatum is a common agricultural and horticultural pest and is one of the host species affected by Phasmarhabditis hermaphrodita

P. hermaphrodita was developed into a natural molluscicide to prevent crop damage from horticultural slug pests from the families Agriolimacidae, Arionidae, Limacidae, Milacidae [4] and Vaginulidae. [18] P. hermaphrodita is the only nematode of the eight families (Agfidae, Alloionematidae, Angiostomatidae, Angiostrongylidae, Cosmocercidae, Diplogasteridae, Mermithidae and Rhabditidae) associated with molluscs, which has been developed as a biological molluscicide, first released under the name Nemaslug® by MicroBio Ltd in 1994, then acquired by Becker Underwood in 2000 and finally taken over by BASF in 2012. [19] Nemaslug® is sold in 15 European countries and is widely used by farmers and gardeners. [20] P. hermaphrodita is currently mass produced in fermenters (up to 20,000 litres (4,400 imperial gallons; 5,300 US gallons)) in a monoxenic liquid broth of the bacterium Moraxella osloensis . [4] In the fields, P. hermaphrodita is applied at 3×10^9 nematodes /ha (1.2×109/acre). [4] Nemaslug® has been found to be successful at reducing agricultural damage from slug in crops such as Winter wheat, lettuce, rapeseed, strawberries, Brussels sprouts, asparagus and others. [4] [21] [22] [23] Even though Nemaslug® takes longer (1–3 weeks) to kill slugs than chemical molluscicides, it has been shown to be equally or more effective at killing slugs. [24] An added advantage to P. hermaphrodita is its ability to strongly suppress feeding of infected slugs [24] and to deter non-infected slugs away from treated soil. [25]

Reproduction and development

Phasmarhabditis hermaphrodita is protandrous autogamous hermaphrodite, [19] whose main substrate to reproduce on is mainly bacterial rich environments such as decomposing cadavers (slugs, snails, worms, insects), leaves, compost and slug faeces. [4] [15] Third stage infective dauers seek out new hosts [12] responding to host cues such as slime and faeces [4] [26] or a bacteria rich environment. Once a new host is found, the dauer enters the slug via the dorsal integumental pouch beneath the mantle and then to the shell cavity via the short canal, [2] [12] next the dauer then develops into a self-fertilizing hermaphrodite and starts to produce young. The mother can produce up to 250–300 young whilst inside their still alive host. [19]

Deroceras reticulatum infected with slug parasitic roundworm Phasmarhabditis hermaphrodita. Deroceras reticulatum infected with roundworm Phasmarhabditis hermaphrodita.jpg
Deroceras reticulatum infected with slug parasitic roundworm Phasmarhabditis hermaphrodita.

At this stage, depending on temperature, the weight of the gastropod, nematode density in the soil the host may die within 4 to 21 days, [2] [4] however, studies show if large enough (over 1g), some slugs (e.g. Arion lusitanicus ) can resist infection. [4] [23] The process involved in killing the host is still not fully understood, whether it is due to internal damage from new offspring or the releasing of M. osloensis. [12] M. osloensis was found growing cultures of P. hermaphrodita [23] and was shown to kill slugs when injected in large amounts into D. reticulatum, [12] but it is not vertically transmitted to offspring, hence its role in the pathogenicity process is currently unclear. [27] When infected by P. hermaphrodita both morphological and behavioural characteristics of the slug change. Morphological changes include a swelling of the mantle area, where both fluid and reproducing nematodes accumulate. [2] Behavioral changes include the fact that infected slugs will be more attracted to areas with populations of P. hermaphrodita, increasing the reproductive fitness of the nematode. [28]

Infected slugs will also find secluded places to die, such as cracks in the soil where they can move down into and conceal themselves deeper within the soil layer. [29] This is theorised to be P. hermaphrodita manipulating the host to go to a more favourable environment. This ensures that they are left alone with the cadaver and avoid any interference with scavengers. [30] The soil also helps to prevent the cadaver from drying out, which creates a moist environment that promotes diverse bacterial growth. [31] Reproduction occurs and the next generation continues to reproduce until food runs out and more third stage infective dauers are produced and the cycle is repeated. [4]

Images

Adult Female Phasmarhabditis hermaphrodita crawling into slug flesh Phasmarhabditis hermaphrodita crawling into slug flesh.gif
Adult Female Phasmarhabditis hermaphrodita crawling into slug flesh

Related Research Articles

<span class="mw-page-title-main">Biological pest control</span> Controlling pests using other organisms

Biological control or biocontrol is a method of controlling pests, whether pest animals such as insects and mites, weeds, or pathogens affecting animals or plants by using other organisms. It relies on predation, parasitism, herbivory, or other natural mechanisms, but typically also involves an active human management role. It can be an important component of integrated pest management (IPM) programs.

Dauer describes an alternative developmental stage of nematode worms, particularly rhabditids including Caenorhabditis elegans, whereby the larva goes into a type of stasis and can survive harsh conditions. Since the entrance of the dauer stage is dependent on environmental cues, it represents a classic and well studied example of polyphenism. The dauer state is given other names in the various types of nematodes such as ‘diapause’ or ‘hypobiosis’, but since the C. elegans nematode has become the most studied nematode, the term ‘dauer stage’ or 'dauer larvae' is becoming universally recognised when referring to this state in other free-living nematodes. The dauer stage is also considered to be equivalent to the infective stage of parasitic nematode larvae.

<span class="mw-page-title-main">Entomopathogenic nematode</span> Group of thread worms that attack insects

Entomopathogenic nematodes (EPN) 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 bio 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 (EPNs) 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.

<i>Deroceras reticulatum</i> Species of gastropod

Deroceras reticulatum, common names the "grey field slug", "grey garden slug", and "milky slug", is a species of small air-breathing land slug, a terrestrial pulmonate gastropod mollusc in the family Agriolimacidae. This species is an important agricultural pest.

<i>Angiostrongylus cantonensis</i> Species of roundworm

Angiostrongylus cantonensis is a nematode (roundworm) parasite that causes angiostrongyliasis, an infection that is the most common cause of eosinophilic meningitis in Southeast Asia and the Pacific Basin. The nematode commonly resides in the pulmonary arteries of rats, giving it the common name rat lungworm. Snails are the primary intermediate hosts, where larvae develop until they are infectious.

<span class="mw-page-title-main">Slug</span> Shell-less terrestrial gastropod mollusc

Slug, or land slug, is a common name for any apparently shell-less terrestrial gastropod mollusc. The word slug is also often used as part of the common name of any gastropod mollusc that has no shell, a very reduced shell, or only a small internal shell, particularly sea slugs and semi-slugs.

<span class="mw-page-title-main">Nematode</span> Phylum of worms with tubular digestive systems with openings at both ends

The nematodes, roundworms or eelworms constitute the phylum Nematoda. They are a diverse animal phylum inhabiting a broad range of environments. Most species are free-living, feeding on microorganisms, but there are many that are parasitic. The parasitic worms (helminths) are the cause of soil-transmitted helminthiases.

<i>Angiostrongylus vasorum</i> Species of roundworm

Angiostrongylus vasorum, also known as French heartworm, is a species of parasitic nematode in the family Metastrongylidae. It causes the disease canine angiostrongylosis in dogs. It is not zoonotic, that is, it cannot be transmitted to humans.

Moraxella osloensis is a Gram-negative oxidase-positive, aerobic bacterium within the family Moraxellaceae in the gamma subdivision of the purple bacteria.

Xenorhabdus is a genus of motile, gram-negative bacteria from the family of the Morganellaceae. All the species of the genus are only known to live in symbiosis with soil entomopathogenic nematodes from the genus Steinernema.

<i>Purpureocillium lilacinum</i> Species of fungus

Purpureocillium lilacinum is a species of filamentous fungus in the family Ophiocordycipitaceae. It has been isolated from a wide range of habitats, including cultivated and uncultivated soils, forests, grassland, deserts, estuarine sediments and sewage sludge, and insects. It has also been found in nematode eggs, and occasionally from females of root-knot and cyst nematodes. In addition, it has frequently been detected in the rhizosphere of many crops. The species can grow at a wide range of temperatures – from 8 to 38 °C for a few isolates, with optimal growth in the range 26 to 30 °C. It also has a wide pH tolerance and can grow on a variety of substrates. P. lilacinum has shown promising results for use as a biocontrol agent to control the growth of destructive root-knot nematodes.

<i>Deroceras invadens</i> Species of gastropod

Deroceras invadens is a species of air-breathing land slug, a terrestrial pulmonate gastropod mollusc in the family Agriolimacidae. Until 2011, this widely distributed species was known as Deroceras panormitanum, and earlier as Deroceras caruanae or Agriolimax caruanae, but Reise et al. (2011) showed that these names refer to a distinct species of similar external appearance known at that time only from Sicily and Malta. Consequently, although the more widespread species was already well known, it then had to be redescribed under the new name of D. invadens. Genetic evidence has indicated that D. invadens is native in southern Italy, including parts of Sicily, and possibly parts of central Italy. Elsewhere it has been introduced, predominantly within the last 100 years, but its spread has been constrained by cold winter temperatures.

Pasteuria is a genus of mycelial and endospore-forming, nonmotile gram-positive bacteria that are obligate parasites of some nematodes and crustaceans. The genus of Pasteuria was previously classified within the family Alicyclobacillaceae, but has since been moved to the family Pasteuriaceae.

<i>Heterorhabditis megidis</i> Species of roundworm

Heterorhabditis megidis is a species of nematodes in the genus Heterorhabditis. All species of this genus are obligate parasites of insects, and some are used as biological control agents for the control of pest insects.

Skrjabingylus nasicola is a species of parasitic nematode in the family Metastrongylidae. Its lifecycle includes an intermediary mollusc host and a paratenic host, a shrew or small rodent. Adult worms are found in the nasal sinuses of mustelids.

Phasmarhabditis californica is a nematode in the family Rhabditidae. It is a lethal facultative parasite of terrestrial gastropods.

Phasmarhabditis (Greek: Phasma = (φάσμα ; rhabditis = is a genus of bacterial-feeding nematodes which are facultative parasites whose primary hosts are terrestrial gastropods. The name comes from Greek: Phasma- (φάσμα ; rhabditis = rod-like (ῥάβδος. The genus is made up of 18 species including P. hermaphrodita, P. californica, P. neopapillosa, P. papillosa, P. apuliae, P. bohemica, P. bonaquaense, P. huizhouensis, P. nidrosiensis, P. valida and P. tawfiki.

Phasmarhabditis neopapillosa is a nematode in the family Rhabditidae. It is a lethal facultative parasite of the terrestrial gastropods.

<i>Steinernema carpocapsae</i> Species of roundworm

Steinernema carpocapsae is an entomopathogenic nematode and a member of the family Steinernematidae. It is a parasitic roundworm that has evolved an insect-killing symbiosis with bacteria, and kills its hosts within a few days of infection. This parasite releases its bacterial symbiont along with a variety of proteins into the host after infection, and together the bacteria and nematode overcome host immunity and kill the host quickly. As a consequence, S. carpocapsae has been widely adapted for use as a biological control agent in agriculture and pest control. S. carpocapsae is considered a generalist parasite and has been effectively used to control a variety of insects including: Webworms, cutworms, armyworms, girdlers, some weevils, and wood-borers. This species is an example of an "ambush" forager, standing on its tail in an upright position near the soil surface and attaching to passing hosts, even capable of jumping. As an ambush forager, S. carpocapsae is thought to be especially effective when applied against highly mobile surface-adapted insects. S. carpocapsae can sense carbon dioxide production, making the spiracles a key portal of entry into its insect hosts. It is most effective at temperatures ranging from 22–28 °C (72–82 °F).

Necromeny is a symbiotic relationship where an animal infects a host and waits inside its body until its death, at which point it develops and completes its life-cycle on the cadaver, feeding on the decaying matter and the subsequent bacterial growth. As the necromenic animal benefits from the relationship while the host is unharmed, it is an example of commensalism.

References

  1. 1 2 3 4 Genena, M. A., Mostafa, F. A., Fouly, A. H., & Yousef, A. A. (2011). First record for the slug parasitic nematode, Phasmarhabditis hermaphrodita (Schneider) in Egypt. Archives of Phytopathology and Plant Protection, 44(4), 340-345.
  2. 1 2 3 4 5 6 Wilson, M. J.; Glen, D. M.; George, S. K. (January 1993). "The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs". Biocontrol Science and Technology. 3 (4): 503–511. doi:10.1080/09583159309355306.
  3. ↑ "Nemaslug®". BASF . 16 January 2017. Archived from the original on 16 January 2017. Retrieved 8 May 2022.
  4. 1 2 3 4 5 6 7 8 9 10 Rae, R., Verdun, C., Grewal, P. S., Robertson, J. F., & Wilson, M. J. (2007). Biological control of terrestrial molluscs using Phasmarhabditis hermaphrodita—progress and prospects. Pest Management Science, 63(12), 1153-1164.
  5. ↑ De Ley, I. T., McDonnell, R. D., Lopez, S., Paine, T. D., & De Ley, P. (2014). Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae), a potential biocontrol agent isolated for the first time from invasive slugs in North America. Nematology, 16(10), 1129-1138.
  6. ↑ Lee, D. L. (Ed.). (2002). The biology of nematodes. CRC Press. 191-191; 294-295
  7. ↑ Wilson, M. J., Glen, D. M., George, S. K., & Butler, R. C. (1993). Mass cultivation and storage of the rhabditid nematode Phasmarhabditis hermaphrodita, a biocontrol agent for slugs. Biocontrol Science and Technology, 3(4), 513-521.
  8. ↑ Maupas, E, (1900) Modes et formes de reproduction des nématodes. Archives de Zoologie Expérimentale et Générale 7, 563-628.
  9. 1 2 Riddle, D. L., & Albert, P. S. (1997). 26 Genetic and Environmental Regulation of Dauer Larva Development. Cold Spring Harbor Monograph Archive, 33, 739-768.
  10. ↑ Ludewig, A. H., Kober-Eisermann, C., Weitzel, C., Bethke, A., Neubert, K., Gerisch, B., ... & Antebi, A. (2004). A novel nuclear receptor/coregulator complex controls C. elegans lipid metabolism, larval development, and aging. Genes & development, 18(17), 2120-2133.
  11. ↑ Tan, L., & Grewal, P. S. (2001a). Infection behavior of the rhabditid nematode Phasmarhabditis hermaphrodita to the grey garden slug Deroceras reticulatum. Journal of Parasitology, 87(6), 1349-1354.
  12. 1 2 3 4 5 Tan, L., & Grewal, P. S. (2001b). Pathogenicity of Moraxella osloensis, a bacterium associated with the nematode Phasmarhabditis hermaphrodita, to the slug Deroceras reticulatum. Applied and Environmental Microbiology, 67(11), 5010-5016.
  13. 1 2 Hooper, D. J., Wilson, M. J., Rowe, J. A., & Glen, D. M. (1999). Some observations on the morphology and protein profiles of the slug-parasitic nematodes Phasmarhabditis hermaphrodita and P. neopapillosa (Nematoda: Rhabditidae). Nematology, 1(2), 173-182.
  14. ↑ Azzam, K. M. (2003). Description of the nematode Phasmarhabditis tawfiki n. sp. isolated from Egyptian terrestrial snails and slugs. JOURNAL-EGYPTIAN GERMAN SOCIETY OF ZOOLOGY, 42(D), 79-88.
  15. 1 2 Wilson, M., & Rae, R. (2015). Phasmarhabditis hermaphrodita as a Control Agent for Slugs. In Nematode Pathogenesis of Insects and Other Pests. 509-521. Springer International Publishing.
  16. ↑ Williams, A. J., & Rae, R. (2015). Susceptibility of the Giant African Snail (Achatina fulica) exposed to the gastropod parasitic nematode Phasmarhabditis hermaphrodita. Journal of invertebrate pathology, 127, 122-126.
  17. 1 2 Nicholls, C. (2014) Implications of not controlling slugs in oilseed rape and wheat in the UK. Research Review No. 79. [PDF] Kenilworth: Agricultural & Horticulture Development Board. 4-5.
  18. ↑ Grewal, S. K., Grewal, P. S., & Hammond, R. B. (2003). Susceptibility of North American native and non-native slugs (Mollusca: Gastropoda) to Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae). Biocontrol Science and Technology, 13(1), 119-125.
  19. 1 2 3 Pieterse, A., Malan, A. P., & Ross, J. L. (2016). Nematodes that associate with terrestrial molluscs as definitive hosts, including Phasmarhabditis hermaphrodita (Rhabditida: Rhabditidae) and its development as a biological molluscicide. Journal of Helminthology, 1-11.
  20. ↑ Iglesias, J., Castillejo, J., & Castro, R. (2003). The effects of repeated applications of the molluscicide metaldehyde and the biocontrol nematode Phasmarhabditis hermaphrodita on molluscs, earthworms, nematodes, acarids and collembolans: a two‐year study in north‐west Spain. Pest management science, 59(11), 1217-1224.
  21. ↑ Wilson, M. J., Glen, D. M., George, S. K., Pearce, J. D., & Wiltshire, C. W. (1994). Biological control of slugs in winter wheat using the rhabditid nematode Phasmarhabditis hermaphrodita. Annals of Applied Biology, 125(2), 377-390.
  22. ↑ Wilson, M. J., Hughes, L. A., Hamacher, G. M., Barahona, L. D., & Glen, D. M. (1996). Effects of soil incorporation on the efficacy of the rhabditid nematode, Phasmarhabditis hermaphrodita, as a biological control agent for slugs. Annals of It can only kill slugs and snails and does not harm non-target organisms like earthworms, insects & acarids. Other methods of slug control include chemical molluscicides such as metaldehyde, iron phosphate and carbamate compounds (Methiocarb and Thiodicarb) have been shown to cause damage to many beneficial/non-beneficial non-target organisms including mammals.applied biology, 128(1), 117-126.
  23. 1 2 3 Wilson, M. J., Glen, D. M., George, S. K., & Hughes, L. A. (1995). Biocontrol of slugs in protected lettuce using the rhabditid nematode Phasmarhabditis hermaphrodita. Biocontrol Science and technology, 5(2), 233-242
  24. 1 2 Lacey, L. A., & Kaya, H. K. (2007). Field manual of techniques in invertebrate pathology. Dordrecht etc.: Kluwer acad. publ. Cop. 2000. 789–790.
  25. ↑ Wilson, M. J., Hughes, L. A., Jefferies, D., & Glen, D. M. (1999). Slugs (Deroceras reticulatum and Arion ater agg.) avoid soil treated with the rhabditid nematode Phasmarhabditis hermaphrodita. Biological Control, 16(2), 170-176.
  26. ↑ Hapca, S., Crawford, J., Rae, R., Wilson, M., & Young, I. (2007). Movement of the parasitic nematode Phasmarhabditis hermaphrodita in the presence of mucus from the host slug Deroceras reticulatum. Biological Control, 41(2), 223-229.
  27. ↑ Rae, R. G., Tourna, M., & Wilson, M. J. (2010). The slug parasitic nematode Phasmarhabditis hermaphrodita associates with complex and variable bacterial assemblages that do not affect its virulence. Journal of invertebrate pathology, 104(3), 222-226.
  28. ↑ Morris, Alex; Green, Michael; Martin, Hayley; Crossland, Katie; Swaney, William T.; Williamson, Sally M.; Rae, Robbie (1 June 2018). "A nematode that can manipulate the behaviour of slugs" (PDF). Behavioural Processes. 151: 73–80. doi:10.1016/j.beproc.2018.02.021. ISSN   0376-6357. PMID   29499346. S2CID   4854918 . Retrieved 9 March 2022.
  29. ↑ Pechova, H., & Foltan, P. (2008). The parasitic nematode Phasmarhabditis hermaphrodita defends its slug host from being predated or scavenged by manipulating host spatial behaviour. Behavioural processes, 78(3), 416-420.
  30. ↑ Foltan, P., & Puza, V. (2009). To complete their life cycle, pathogenic nematode–bacteria complexes deter scavengers from feeding on their host cadaver. Behavioural processes, 80(1), 76-79.
  31. ↑ Rae, R. G., Tourna, M., & Wilson, M. J. (2010). The slug parasitic nematode Phasmarhabditis hermaphrodita associates with complex and variable bacterial assemblages that do not affect its virulence. Journal of invertebrate pathology, 104(3), 225-226.

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