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Phasmarhabditis (syn. Pellioditis) californica is a facultative parasite that has been marketed as a popular biocontrol agent against pestiferous slugs in England, Scotland, and Wales. The necromenic nematode Pristionchus entomophagus has also been recovered from slugs infected with Ph. californica. In this study, we experimentally investigated the outcome of single and mixed applications of Pr. entomophagus and Ph. californica on the slug Deroceras reticulatum (Müller). Host mortality was comparable for single and mixed applications of Ph. californica, with time to death significantly shorter in both treatment groups compared with controls. However, trials with Pr. entomophagus alone did not cause any significant host mortality relative to controls. Compared with the single Ph. californica applications, mixed applications resulted in 67% fewer infective juveniles establishing in the host, and subsequently far fewer infective juveniles were recovered in the next generation. In contrast, the establishment rate and progeny production in Pr. entomophagus were not impacted by the presence of Ph. californica (i.e., mixed applications). Hence, the presence of Pr. entomophagus had a deleterious effect on the establishment success and progeny production of Ph. californica. Our findings reveal an asymmetrical, antagonistic interaction between Ph. californica and Pr. entomophagus and highlight the importance of understanding the ecological relationships between co-occurring species. A decrease in parasite establishment success and progeny production has the potential to directly impact the persistence, sustainability, and efficacy of Ph. californica as a biological control agent., (© American Society of Parasitologists 2024.)

The gastropod parasitic nematode Phasmarhabditis hermaphrodita has been formulated into a successful biological control agent (Nemaslug®, strain DMG0001) used to kill slugs on farms and gardens. When applied to soil, P. hermaphrodita uses slug mucus and faeces to find potential hosts. However, there is little information on what cues other species of Phasmarhabditis (P. neopapillosa and P. californica) use to find hosts and whether there is natural variation in their ability to chemotax to host cues. Therefore, using chemotaxis assays, we exposed nine wild isolates of P. hermaphrodita, five isolates of P. neopapillosa and three isolates of P. californica to mucus from the pestiferous slug host Deroceras invadens, as well as 1% and 5% hyaluronic acid - a component of slug mucus that is highly attractive to these nematodes. We found P. hermaphrodita (DMG0010) and P. californica (DMG0018) responded significantly more to D. invadens mucus and 1% hyaluronic acid than other strains. Also, P. hermaphrodita (DMG0007), P. neopapillosa (DMG0015) and P. californica (DMG0017) were superior at locating 5% hyaluronic acid compared to other isolates of the same genera. Ultimately, there is natural variation in chemoattraction in Phasmarhabditis nematodes, with some strains responding significantly better to host cues than others.

The Spanish Slug (Arion vulgaris, formerly known as Arion lusitanicus) is an invasive agricultural and horticultural pest species that causes great damages all over Europe. Numerous options to control this slug are on the market; among the most commonly used are slug pellets containing the active ingredients metaldehyde or iron-III-phosphate and the application of parasitic nematodes (Phasmarhabditis hermaphrodita). These control measures potentially also affect non-target organisms like earthworms (Lumbricidae), which themselves can directly and/or indirectly alter a plant's susceptibility against slug herbivory. Also, the efficacy of slug control treatments is expected to be influenced by watering. In a greenhouse experiment we investigated the influence of daily watering vs. every third day watering on slug control efficacy and potential interactions with earthworms. We found significant interactions between watering and slug control efficacy. Slug herbivory and biomass decreased after application of slug pellets; metaldehyde was more effective under less frequent watering while iron-III-phosphate was unaffected by watering. Parasitic nematodes had no effect on slug herbivory and biomass production. Earthworm activity was reduced with less frequent watering but did not interact with slug control. We conclude that watering patterns should be considered when choosing slug control measures.

Phasmarhabditis hermaphrodita is a parasitic nematode of terrestrial gastropods that has been formulated into a biological control agent for farmers and gardeners to kill slugs and snails. In order to locate slugs it is attracted to mucus, faeces and volatile cues; however, there is no information about whether these nematodes are attracted to snail cues. It is also unknown how wild isolates of P. hermaphrodita or different Phasmarhabditis species behave when exposed to gastropod cues. Therefore, we investigated whether P. hermaphrodita (commercial and wild isolated strains), P. neopapillosa and P. californica were attracted to mucus from several common snail species (Cepaea nemoralis, Cepaea hortensis, Arianta arbustorum and Cornu aspersum). We also examined whether snails (C. aspersum) collected from different locations around the UK differed in their attractiveness to wild isolates of P. hermaphrodita. Furthermore, we also investigated what properties of snail mucus the nematodes were attracted to, including hyaluronic acid and metal salts (FeSO4, ZnSO4, CuSO4 and MgSO4). We found that the commercial strain of P. hermaphrodita responded poorly to snail mucus compared to wild isolated strains, and C. aspersum collected from different parts of the UK differed in their attractiveness to the nematodes. We found that Phasmarhabditis nematodes were weakly attracted to all metals tested but were strongly attracted to hyaluronic acid. In a final experiment we also showed that pharmacological manipulation of cyclic guanosine monophosphate (cGMP) increased chemoattraction to snail mucus, suggesting that the protein kinase EGL-4 may be responsible for Phasmarhabditis sp. chemoattraction.

This study investigated the possible biological, biochemical and histological changes in Bradybaena similaris(Gastropoda: Pulmonata) infected by Heterorhabditis indica (Rhabditida: Heterorhabditidae), strain LPP1. Two groups of 16 snails were formed: the control group (unexposed) and the treated group, which was exposed for three weeks to infective juveniles (J 3 ) of H. indica LPP1. The experiment was conducted in duplicate, using a total of 64 snails. After the exposure period, the snails were dissected to collect the hemolymph and tissues, for evaluation of the physiological changes caused by the infection. The number of eggs laid/snail and the viability of these eggs were also assessed as indicators of the reproductive activity of B. similaris. Intense glycogenolysis was accompanied by a significant reduction (p < 0.05) in the glucose content of the hemolymph of the exposed snails, indicating that infection by H. indica induces breakdown of the host's glycemic homeostasis. Significant variations (p < 0.05) in the lactate dehydrogenase activity occurred together with changes in the concentration of pyruvic and lactic acid in the hemolymph of the infected B. similaris snails, corroborating the transition from aerobic to anaerobic metabolism in the hosts. These metabolic alterations reflect the parasitic castration process in this interface. The results suggest that the use of H. indica LPP1 is a potential alternative for biological control of B. similaris., (Copyright © 2017 Elsevier Inc. All rights reserved.)

The dynamics of predation on parasites within prey has received relatively little attention despite the profound effects this is likely to have on both prey and parasite numbers and hence on biological control programmes where parasites are employed. The nematode Phasmarhabditis hermaphrodita is a commercially available biological agent against slugs. Predation on these slugs may, at the same time, result in intraguild predation on slug-parasitic nematodes. This study describes, for the first time, predation by carabid beetles on slugs and their nematode parasites on both spatial and temporal scales, using PCR-based methods. The highest nematode infection levels were found in the slugs Deroceras reticulatum and Arion silvaticus. Numbers of infected slugs decreased over time and no infected slugs were found four months after nematode application. The density of the most abundant slug, the invasive Arion vulgaris, was positively related to the activity-density of the carabid beetle, Carabus nemoralis. Predation on slugs was density and size related, with highest predation levels also on A. vulgaris. Predation on A. vulgaris decreased significantly in summer when these slugs were larger than one gram. Predation by C. nemoralis on slugs was opportunistic, without any preferences for specific species. Intraguild predation on the nematodes was low, suggesting that carabid beetles such as C. nemoralis probably do not have a significant impact on the success of biological control using P. hermaphrodita.

Phasmarhabditis hermaphrodita is a nematode parasite of slugs that is commercially reared in monoxenic culture with the bacterium Moraxella osloensis and sold as a biological molluscicide. However, its bacterial associations when reared in vivo in slugs are unknown. We show that when reared in vivo in slugs, P. hermaphrodita does not retain M. osloensis and associates with complex and variable bacterial assemblages that do not influence its virulence. This is in marked contrast to the entomopathogenic nematodes that form highly specific mutualistic associations with Enterobacteriaceae that are specifically retained during in vivo growth., ((c) 2010 Elsevier Inc. All rights reserved.)

Phasmarhabditis hermaphrodita is a parasitic nematode that has been formulated into a biological control agent for slugs. The nematode responds to slug-associated cues such as mucus and feces in order to locate potential hosts. We assessed the olfactory response of P. hermaphrodita to mucus from 9 species of slugs, 2 snails, and 2 earthworms (non-hosts). We then examined the susceptibility of each invertebrate test species to high doses of P. hermaphrodita to determine whether susceptible species are more attractive than non-susceptible species to the nematode. We also studied the numbers of infective juveniles produced in each test species, as well as infectivity. Phasmarhabditis hermaphrodita showed strong attraction to mucus from the non-susceptible slug Arion subfuscus, the snail Helix aspersa, and the highly susceptible slug Deroceras reticulatum. In reproduction experiments, P. hermaphrodita produced the highest number of infective juveniles in D. reticulatum and Deroceras panormitanum; however, there was no significant relationship with attraction. Phasmarhabditis hermaphrodita caused significant mortality in 5-11 gastropod species tested (and showed no chemotactic preference for susceptible or non-susceptible species). There was a significant positive relationship between numbers of P. hermaphrodita penetrating into non-susceptible species and chemotaxis response. These necromenic species represent ideal hosts for P. hermaphrodita in terms of providing protection against abiotic and biotic factors as well as transport to many diverse areas.

Background: Controlling pests through disruption of biochemical pathways by physiologically active compounds/factors from animals and plants represents an expanding field of research. The authors investigated whether such factors in venom from the wasp Pimpla hypochondriaca (Retzius) can affect the viability and food consumption of the slug Deroceras reticulatum (Müller), and whether they can improve the efficacy of nematode-induced slug mortality., Results: Exposure of slugs to 4 mL of water containing 500, 1000 and 5000 Phasmarhabditis hermaphrodita (Schneider) resulted in significant increases in mortality (with hazard ratios of 3.5, 3.9 and 5.8 respectively) and significant reductions in total food consumption and mean food consumption each day for 21 days. Injection of slugs with 4, 8 or 12 microL of P. hypochondriaca venom resulted in significant increases in mortality (with hazard ratios of 3.3, 4.5 and 9.0 respectively) and significant reductions in total food consumption compared with the controls. However, there was no significant effect of venom on the mean food consumption on individual days of the 21 day assay period, although significant reductions occurred for the 8 and 12 microL doses up to day 10. Injecting slugs with 4 microL of venom prior to exposure to 500 nematodes had no synergistic effect on either mortality or food consumption compared with either of the individual treatments., Conclusions: Pimpla hypochondriaca venom contains factors capable of killing and reducing food consumption by D. reticulatum. The utilization of these factors as components of integrated pest management strategies is discussed.

Infective stages of commercially used molluscicidal rhabditide nematodes Phasmarhabditis hermaphrodita contain bacterial symbionts which kill their host by septicaemia. The nematodes feed on the multiplying bacteria and entire host tissue, develop and repeatedly reproduce. Invertebrate cadavers are rapidly (from minutes to hours) removed by scavengers. However nematodes need days to complete their life cycle inside the host. The post mortem locations of slugs killed by six different treatments (three types of molluscicides, a simulation of unsuccessful predation and two P. hermaphrodita nematode treatments) were compared. In comparison to other pathogenic states, significantly more slugs killed by the nematodes died within the soil, where the scavenging pressure is weaker than on the soil surface (where most of the slugs died regardless treatment). We suggest that this is an outcome of behavioural manipulation, which prevent the parasites from being predated or scavenged together with their host until the nematodes complete development inside the host cadaver.