Thirty years of slug control using the parasitic nematode Phasmarhabditis hermaphrodita and beyond.

Several slug species are highly pestiferous and threaten global sustainable agriculture. Current control methods rely heavily on metaldehyde pellets, which are often ineffective, harm nontarget organisms and have been banned in some countries. A viable alternative is the parasitic nematode Phasmarhabditis hermaphrodita (and recently P. californica), which has been formulated into a biological control agent (Nemaslug®) to control slugs across northern Europe. Nematodes are mixed with water and applied to soil where they seek out slugs, penetrate behind the mantle and kill them in 4-21 days. Phasmarhabditis hermaphrodita has been on the market since 1994 and since then there has been ample research on its use. Here we review the research carried out on P. hermaphrodita over the last 30 years since its development and release as a commercial product. We provide information on life cycle, worldwide distribution, history of commercialisation, gastropod immunity, host range, ecological and environmental factors that affect its success in the field, bacterial relationships, and summarise results of field trials. Finally, we suggest future directions for P. hermaphrodita research (and other Phasmarhabditis species) to enhance its use as a biological control agent to control slugs for the next 30 years. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

A parasitic nematode induces dysbiosis in susceptible but not resistant gastropod hosts.

Animals' gut microbiomes affect a wide array of biological processes including immunity and protection from pathogens. However, how the microbiome changes due to infection by parasites is still largely unknown, as is how the microbiome changes in hosts that differ in their susceptibility to parasites. To investigate this, we exposed two slug species of differing susceptibility to the parasitic nematode Phasmarhabditis hermaphrodita (Deroceras reticulatum is highly susceptible and Ambigolimax valentianus resistant to the nematode) and profiled the gut microbiota after 7 and 14 days. Before infection, both slug species' microbiota was dominated by similar bacterial genera: Pseudomonas (by far the most abundant), Sphingobacterium, Pedobacter, Chryseobacterium, and Flavobacterium. In the resistant host A. valentianus, there was no significant change in the bacterial genera after infection, but in D. reticulatum, the bacterial profile changed, with a decrease in the abundance of Pseudomonadaceae and an increase in the abundance of Flavobacteriaceae and Sphingobacteriaceae after 7 days postinfection. This suggests nematode infection causes dysbiosis in hosts that are susceptible to infection, but the microbiome of resistant species remains unaltered. In summary, the regulation of the immune system is tightly linked with host survival, and nematode infection can alter the microbiome structure.

Microbiome Analysis of Malacopathogenic Nematodes Suggests No Evidence of a Single Bacterial Symbiont Responsible for Gastropod Mortality.

Nematodes and bacteria are prevalent in soil ecosystems, and some have evolved symbiotic relationships. In some cases, symbionts carry out highly specialized functions: a prime example being entomopathogenic nematodes (EPNs), which vector bacteria (Xenorhabdus or Photorhabdus) into insect hosts, killing them to provide a food source for the nematodes. It is thought that the commercially available malacopathogenic (kills slugs and snails) biocontrol nematode Phasmarhabditis hermaphrodita vectors a bacterium (Moraxella osloensis) into slugs to kill them. To investigate this further we used a metagenomic approach to profile the bacteria present in the commercial strain of P. hermaphrodita, a wild strain of P. hermaphrodita and two other Phasmarhabditis species (P. californica and P. neopapillosa), after they had killed their slug host (Deroceras invadens). We show that these nematodes do not exclusively associate with one bacterium but a range of species, with members of the phyla Pseudomonadota, Bacillota, Actinobacteriota and Bacteroidota the most prevalent. The commercial strain of P. hermaphrodita had the least diverse bacterial community. Furthermore, we found that the bacterium P. hermaphrodita has been cultured on for 25 years is not the expected species M. osloensis but is Psychrobacter spp. and the only strain of the Phasmarhabditis species to associate with Psychrobacter spp. was the commercial strain of P. hermaphrodita. In summary, we found no evidence to show that P. hermaphrodita rely exclusively on one bacterium to cause host mortality but found variable and diverse bacterial communities associated with these nematodes in their slug hosts.