Figure 20 - uploaded by Rory J Mc Donnell
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Arion lusitanicus Mabille (= vulgaris Moquin-Tandon) in copula. Species not yet reported from the United States, but likely to be collected in the future. A very serious agricultural pest elsewhere. Photograph by Roy Anderson.
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The Significance of Alien and Invasive Slug Species for Plant Communities in Agrocenoses
This paper lists alien invasive species of slugs occurring on crops grown in the ground and under covers, as well as in adjacent habitats. It gives a description of their origin, distribution within Poland, frequency of occurrence in different habitats, and an...
Citations
... Deroceras reticulatum were collected from various grass seed production fields throughout the Willamette Valley, OR, USA. Field-collected slugs were identified and confirmed as D. reticulatum using [34,35]. Slugs were not cultured in the laboratory. ...
... In total, 228 immunity-related genes (Log2 fold > 2) were identified and categorized into 10 different groups, such as signal transduction (86 genes), scavenger receptor (34 genes), immunoglobulin family protein (23 genes), sialic acid protein (22 genes), c-Jun N-terminal kinase (JNK) (21 genes), C-type lectin-like domain (CTLD) protein (19 genes), dual oxidase (Duox) (10 genes), toll-like receptor (TLR) (8 genes), bactericidal permeabilityincreasing protein (BPI) (3 genes), and CD109 antigen-like (2 genes), respectively. Among the immunity-related genes, signal transduction (86) were the most abundant DEGs followed by scavenger receptors (34) in the nematode-infected slug compared to the control slug ( Figure 5 and File S1). ...
... In total, 228 immunity-related genes (Log2 fold > 2) were identified and categorized into 10 different groups, such as signal transduction (86 genes), scavenger receptor (34 genes), immunoglobulin family protein (23 genes), sialic acid protein (22 genes), c-Jun N-terminal kinase (JNK) (21 genes), C-type lectin-like domain (CTLD) protein (19 genes), dual oxidase (Duox) (10 genes), toll-like receptor (TLR) (8 genes), bactericidal permeability-increasing protein (BPI) (3 genes), and CD109 antigen-like (2 genes), respectively. Among the immunity-related genes, signal transduction (86) were the most abundant DEGs followed by scavenger receptors (34) in the nematode-infected slug compared to the control slug ( Figure 5 and File S1). ...
The grey garden slug (Deroceras reticulatum), a common terrestrial slug native to Europe with a global distribution including North America, is commonly considered the most severe slug pest in agriculture. The nematode Phasmarhabditis hermaphrodita, which has been used in the U.K. and Europe as a commercial biocontrol agent since 1994, has also recently been collected in Oregon and California and has long been considered a candidate biocontrol agent for slug management in the U.S. In this study, we report differential gene expressions in nematode-infected slugs using RNA-seq to identify slug immune-related genes against nematodes. Comparison of gene expression levels between the whole bodies of a nematode-infected slug (N-S) and an uninfected control slug (C-S) revealed that there were a total of 39,380 regulated unigenes, of which 3084 (3%) were upregulated and 6761 (6%) were downregulated at greater than 2-fold change (FC > 2) in the nematode-infected slug. To further investigate the biological functions of differentially expressed genes (DEGs), gene ontology (GO) and functional enrichment analysis were performed to map the DEGs to terms in the GO, eukaryotic ortholog groups of proteins (KOG) and Kyoto Encyclopedia of Genes and Genome Pathway (KEGG) databases. Among these DEGs, approximately 228 genes associated with immunity or immune-related pathways were upregulated 2-fold or more in the N-S compared to C-S. These genes include toll, Imd, JNK, scavenger receptors (SCRs), C-type lectins (CTLs), immunoglobulin-like domains, and JAK/STAT63 signaling pathways. From the RNA-seq results, we selected 18 genes and confirmed their expression levels by qRT-PCR. Our findings provide insights into the immune response of slugs during nematode infection. These studies provide fundamental information that will be valuable for the development of new methods of pest slug control using pathogenic nematodes in the field.
... Purposive, nonprobability sampling (Bhardwaj 2019) was done based on the animal's selectivity towards favourable micro-habitats (such as moist, cool spaces underneath leaf litter and in between rock rubbles, pieces of wood, etc.). Identification of the slugs and snails was based on morphology (Kerney et al. 1979;Mc Donnell et al. 2009;Thomas et al. 2010). The collected slugs and snails were placed in plastic containers lined with tissue paper and stored at 4°C. ...
A survey for slug- and snail-associated nematodes was conducted in forests, parks, botanical gardens, and nature reserves at 13 localities in Belgium to uncover more diversity of gastropod mollusc-associated nematodes and to characterise Pellioditis populations found in the country. A total of 319 slugs and snails belonging to nine species were examined. Arion vulgaris was the most commonly found mollusc species in this study (eight locations), and 19.4% of the examined mollusc specimens were found infected by nematodes. The highest prevalence of nematodes was observed in Cornu aspersum (60%) followed by A. vulgaris (34.8%), Limax maximus (28.6%), and Cepaea sp. (20%). Eleven nematode species belonging to eight families were isolated and identified from the mollusc hosts including Alloionema appendiculatum , Angiostoma dentiferum , A. gandavense , Angiostrongylus vasorum , Cosmocerca longicauda , Panagrolaimus cf. subelongatus , Pellioditis californica , P. hermaphrodita , Rhabditis sp., Tetrameres cf. fissispina , and Troglostrongylus cf. brevior. Pellioditis was the most commonly found nematode genus (at nine localities) and C. longicauda and P. californica were reported in Belgium for the first time. Co-infections of more than one nematode species were observed in eight (2.5%) molluscs specimens. Most co-infections consisted of two nematode species. In one A. vulgaris specimen, a co-infection of three nematode species ( A. vasorum , P. hermaphrodita , and Tetrameres cf. fissispina ) was observed. Four ex vivo cultures of P. californica and six ex vivo cultures of P. hermaphrodita were established from single hermaphrodites, and both species were described based on light microscopy, scanning electron microscopy, and morphometric, morphological, and molecular data.
... Given such opportunities, these species can spread rapidly and even become invasive (Kozłowski and Kozłowski 2011;Wiktor 2001). Pest gastropods cause significant economic damage to crops in many countries (Baker 2002;Bishop 1977;Carlos Villalobos et al. 1995;Godan 1983;Kozłowski and Kozłowski 2011;Mc Donnell et al. 2009). In addition, these pests lower the quality of the crops by soiling them with slime and feces and can transmit pathogens or their eggs to plants, humans and livestock (Kozłowski 2012). ...
Background: The available information on terrestrial pest gastropods and their impact on the environment worldwide is scarce and outdated. The present study aimed to address this gap by conducting the first comprehensive survey of pest gastropods in the Nuwara Eliya District, an important vegetable growing area in the highlands of Sri Lanka. Eighty agricultural lands were surveyed over two years by establishing ten 1 m2 sampling plots per crop type in each agricultural land. Geo-coordinates, air temperature, elevation, relative humidity, daily rainfall, soil pH, species richness and abundance were recorded for rainy and non-rainy periods. The relationship between species composition and environmental variables was analyzed using multi-regression models and distribution maps.
Results: Out of the 14 species recorded in agricultural lands, nine were identified as exotic pest species. Species abundance (t = 4.69, p < 0.05) and diversity was higher in the rainy period and the dominant species during this period were Bradybaena similaris (t = 2.69, p < 0.05) and Deroceras reticulatum (t = 2. 46, p < 0.05). Eggs and estivating adults were found in soil and under decaying organic matter during the non-rainy period. The exotic species showed broader preferences for the measured environmental factors and showed a wider range in distribution compared to the native species. Variation in pest gastropod composition was significantly accounted for by elevation, relative humidity, soil pH and daily rainfall. Additionally, the species richness and abundance varied across locations due to the combined effects of elevation, crop type and stage, and field type.
Conclusions: The study emphasizes the importance of understanding the biology and ecology of gastropod pests to develop effective management strategies. By considering the influence of environmental factors and implementing appropriate soil management techniques, such as targeting specific habitats and crop stages, it is possible to mitigate pest populations and minimize their impact on agricultural lands. Overall, this research contributes valuable insights into the dynamics and interactions of terrestrial gastropods in agricultural ecosystems, supporting sustainable pest management practices.
... Purposive, nonprobability sampling (Bhardwaj 2019) was done based on the animal's selectivity towards favourable micro-habitats (such as moist, cool spaces underneath leaf litter and in between rock rubbles, pieces of wood, etc.). Identification of the slugs and snails was based on morphology (Kerney et al. 1979;Mc Donnell et al. 2009;Thomas et al. 2010). The collected slugs and snails were placed in plastic containers lined with tissue paper and stored at 4°C. ...
... Independent studies in other geographic regions have also recorded the presence of pest gastropods such as Lissachatina fulica, Arion sp., Deroceras reticulatum, Deroceras laeve, Milax gagates, and Laevicaulis sp. inside natural forests systems that pose threats to native species [25][26][27][28][29][30][31]. ...
Sri Lanka is home to 253 terrestrial gastropod species, most of which are endemic. However, limited research has explored the diversity, distribution, and influencing variables of these gastropods. This study sampled gastropods in tropical montane rainforests by establishing 10-50 1-m2 sampling plots across 60 randomly selected sites. Among the 46 recorded species, 79% were native, and 17% were exotic. Species representative of the five endemic genera to the island and two endemic semi-slug species were recorded from these forests. Native gastropod species were primarily found in forest interiors, while exotic species inhabited forest buffer regions. The distribution of most native species is influenced by elevation, air temperature, relative humidity, rainfall, and soil pH, while elevation and rainfall play a significant role in the distribution of most exotics. Exotics display broader environmental tolerance compared to natives, enabling exotics to invade the forests. The restricted habitat of many native species within deep canopy forests makes them highly vulnerable to habitat change, whereas exotics thrive under altered conditions.
... Slugs collected from different sampling sites were put into separate containers to avoid any cross-contamination. Each slug species was photographed and identified using available taxonomic keys (Perez et al., 2008;Grimm et al., 2009;Mc Donnell et al., 2009; http://idtools.org/id/mollusc/index.php). Molecular diagnosis for slugs was performed when I could not reliably make an identification using morphological traits, or if the samples contained immature slugs that were difficult to identify solely on external morphologies. ...
Certain slug species are considered agricultural and horticultural pests worldwide. Nematodes offer a potential solution as biocontrol agents in controlling slug populations due to their natural associations with terrestrial gastropods. In some cases, they provide higher specificity and more efficient pest management outputs than many chemical or physical practices currently available. One of the most well-known biocontrol agents of slugs is a facultative parasite, Phasmarhabditis hermaphrodita, which has been widely established as a biocontrol agent after
it was patented and commercialized as a molluscicide product (Nemaslug ® with the associated bacteria symbiont, Moraxella osloensis) in 1994 in the UK. However, Canada had no previous record of any Phasmarhabditis species until a recent discovery of a Canadian strain of P. californica collected from a local nursery in Edmonton, Alberta. This species was originally isolated from California and subsequently marketed by BASF as a biocontrol agent (Nemaslug® 2.0) against slugs in England, Scotland, and Wales in 2022. However, the immediate use of this species as a biocontrol agent is currently not available in Canada until a
proper risk assessment of the biocontrol product Nemaslug 2.0 with the active organisms P. californica (with the bacteria symbiont, Moraxella osloensis) is made and its biology fully understood. First, I conducted an extensive survey to identify the diversity, distribution, and abundance of pest slug species and their associated nematodes in selected agricultural and horticultural sites in Alberta. I further investigated if any Phasmarhabditis species were present in the survey sites. I collected 1331 slugs belonging to nine species, with Deroceras reticulatum being the most common. Forty-five samples (3.38%) were positive for nematodes, the majority were identified to species level: Alloionema appendiculatum, Caenorhabditis briggsae, Caenorhabditis elegans, Panagrolaimus subelongatus, and Mesorhabditis spiculigera. I did not isolate P. californica from any of the slugs collected from these survey sites, which included the original site where P. californica was discovered. However, four D. reticulatum slugs retrieved from a residential garden sample were infected with P. californica, thereby suggesting a
possible fragmented distribution for this strain in the province. I then used an agar-based chemotaxis assay to evaluate the host preference of the laboratory-cultured Canadian strain of P. californica against four pest slug species, D. reticulatum, A. rufus, A. fasciatus, and A. valentianus. I showed that P. californica was strongly attracted to mucus of all slug species except for D. reticulatum for which I observed a weak attraction. In addition, I checked the host preference of a co-occurring nematode, Pristionchus entomophagus, a necromenic nematode on the same host species to check if they would have a similar host preference as P. californica. P.
entomophagus showed a significant attraction to the mucus of D. reticulatum while being strongly repulsive to A. rufus. Given that these two nematode species have potential similarities in chemoattraction profiles towards D. reticulatum, I then investigated the efficacy of the infectivity of P. californica as a biocontrol agent in the presence of P. entomophagus. The ability to cause mortality in slugs infected by P. californica was the same in single and mixed infections, i.e., mortality rates remained the same despite its co-occurrence with P. entomophagus. Both in single and mixed infection treatments, the number of P. californica that entered the slug host also remained comparable and statistically non-significant. However, the
number of progeny (F1) in mixed treatments was lower than that of the single treatments for P. californica. Interestingly, P. entomophagus was not affected by concomitant infection with P. californica. These discoveries on the local strains of Phasmarhabditis support the possibility of using P. californica as a biological control agent within Canada. Still, further investigation is needed on the persistence and efficacy of P. californica in the presence of other nematode species in the soil community
... The three slug species that we captured are invasive species. Exotic populations of D. laeve were probably established in North America in the 1700s but this Holarctic species also has native populations in the U.S. [61]. Deroceras reticulatum was introduced into the USA in the 1800s [62]. ...
Slugs are cryptic terrestrial pests that target a wide range of crops and are especially damaging to seedlings. Management of these invertebrates mostly relies on synthetic chemistry. These molecules can be efficient against slugs and snails but can be toxic to other organisms (e.g., dogs) and harmful to the environment (e.g., leaching into surface and groundwater). The usage of pathogenic nematodes has been effective in several crops and European countries. A survey was conducted to investigate the presence of natural populations of malacopathogenic nematodes in soybean in the mid-Atlantic region. Slugs were sampled in nine fields across Delaware at various distances from the field edges (0 m, 5 m, 10 m, 15 m). Soil cover and soil type were also recorded. Invertebrates were brought back to the laboratory. Slugs were monitored for four weeks, and mortality was classified into one of three categories: (1) death with the presence of nematodes; (2) death with the presence of fungi; (3) death without the presence of nematodes or fungi. Nematodes associated with slugs were identified based on 18S rRNA sequencing. The distance from the field edge did not impact the number of trapped slugs and the incidence of slug death associated with the presence of nematodes. Overall, nematodes were collected from ca. 20% of the slug cadavers, and most have previously been associated with slugs (ca. 35% of deaths associated with fungi and ca. 45% not associated with nematodes or fungi). The number of captured slugs and slug death associated with the presence of nematodes were positively correlated with ground cover. Soil type impacted both the number of captured slugs and the presence of pathogenic nematodes. This survey provides a first insight into the natural populations of mollusk-associated nematodes in the mid-Atlantic region. This knowledge may contribute to implementing cultural practices favoring these natural enemies of slug pests.
... Deroceras laeve (O.F. Muller, 1774), the marsh slug, appears to be native to the United States and has been introduced across the US and the world (McDonnell et al., 2009). This slug speciescan cause significant damage to crop fields, though outbreaks are usually less intense than those of D. reticulatum (Douglas and Tooker, 2012). ...
... We placed 4 shelters haphazardly in each plot, away from plot edges (> 4 m) to avoid edge effects. We counted the number of slugs underneath each shelter (including slugs attached to the bottom of the shelter and on the soil) once a week in the morning (before 10:00 am) from planting through harvest and identified slugs to species in the field as Deroceras reticulatum or D. laeve (Chichester and Getz, 1973;McDonnell et al., 2009). ...
No-till farming is a conservation agriculture practice employed on over 100 million acres of farmland in the United States. This practice provides benefits ranging from erosion control to pest suppression but can also facilitate outbreaks of novel pests. In the Mid-Atlantic, USA, where no-till production is widely adopted to help maintain the health of the Chesapeake Bay watershed, slugs have become a major pest of no-till row crops. Tillage buries slug eggs and kills all life stages; thus, slugs thrive without this interference in no-till systems. Effective slug control options are lacking, but integrating cover crops into crop rotations, especially when delaying termination until after cash crop planting (planting green), could be an ecologically based, cost effective method to control slugs. Cover crops may offer a dual-pronged approach to slug management, conferring top-down control by creating habitat for predators and bottom-up control by acting as a dietary distraction. The goal of the experiment presented here was to understand how delaying cover-crop termination until after cash-crop planting affects top-down and bottom-up control of slugs. Additionally, we assessed the effect of neonicotinoid-coated seeds on top down-control because insecticides can harm predators. Across three commercial, row-crop farms in Pennsylvania, USA, we found that slug activity-density and damage to cash crops was lowest in planting green treatments due to higher residue coverage and that planted-green maize plots without seed coatings had the lowest slug pressure. Planting-green produced lower yields that, given the conservation benefits, may be acceptable to some farmers, and yields were not enhanced by insecticidal seed coating. Collectively, our results indicate that planting-green can act as a novel, bottom-up management strategy for slugs that functions independently of top-down control.
... Some of these introduced gastropods are considered among the most pestiferous slugs and snails. These species include Deroceras reticulatum (Müller 1774), Arion hortensis (Ferrusac 1819), and Cornu aspersum (Müller 1774) (Mc Donnell et al., 2009). For example, C. aspersum can reduce some California citrus fruit crop yields by 40-50% and occasionally up to 90-100% in years of high rainfall (Pappas and Carman, 1961;Sakovich, 2002). ...
Three species of Phasmarhabditis were recovered from 75 nurseries and garden centers in 28 counties in California during fall and winter 2012–2021. A total of 18 mollusk species were recovered, most of them invasive. Nematodes were identified by sequencing the D2-D3 expansion segments of the large subunit (LSU or 28S) rRNA. Based on these surveys, P. californica was the most widespread species (37 isolates, 53.6% recovery); followed by P. hermaphrodita (26 isolates; 37.7% recovery); P. papillosa and a closely related P. papillosa isolate (6 isolates; 8.7% recovery). Nematode isolates were mainly collected from four invasive slugs (Deroceras reticulatum, D. laeve, Arion hortensis agg, Ambigolimax valentianus) and snails (Oxychilus spp. and Discus spp.). Results suggest that P. californica and P. hermaphrodita share an ecological niche in Northern, Central, Coastal, and Southern California, north of Los Angeles County.
... Indeed, their success is attributed to mucus production that deters predators, as well as high reproduction rates and adaptable appetites [4]. They are major pests of plant nurseries and several agricultural crops, including corn, soybean, wheat, brassicas, leafy vegetables, and strawberry crop systems [46]. Slugs target a variety of plants and grasses, often by killing seedlings outright, causing considerable amounts of economic damage in California arable and horticultural crops, commercial nurseries, and home gardens [4,47]. ...
... Most slug species found in California nurseries are invasive, with many having been transported long distances. Known invasive slug species in California include members of genera Deroceras and Arion, as well as the species Milax gagates and Ambigolimax valentianus, all originating from Europe [4,46]. Although individual slugs do not move rapidly per se, trade in horticultural commodities has facilitated their spread. ...
... Although individual slugs do not move rapidly per se, trade in horticultural commodities has facilitated their spread. As a result, additional exotic slug species, or species not considered to be endemic to California, are likely to appear there in the near future [4,46]. ...
Ambigolimax valentianus is an invasive European terrestrial gastropod distributed throughout California. It is a serious pest of gardens, plant nurseries, and greenhouses. We evaluated the bacterial microbiome of whole slugs to capture a more detailed picture of bacterial diversity and composition in this host. We concentrated on the influences of diet and environment on the Ambigolimax valentianus core bacterial microbiome as a starting point for obtaining valuable information to aid in future slug microbiome studies. Ambigolimax valentianus were collected from two environments (gardens or reared from eggs in a laboratory). DNA from whole slugs were extracted and next-generation 16S rRNA gene sequencing was performed. Slug microbiomes differed between environmental sources (garden- vs. lab-reared) and were influenced by a sterile diet. Lab-reared slugs fed an unsterile diet harbored greater bacterial species than garden-reared slugs. A small core microbiome was present that was shared across all slug treatments. This is consistent with our hypothesis that a core microbiome is present and will not change due to these treatments. Findings from this study will help elucidate the impacts of slug-assisted bacterial dispersal on soils and plants, while providing valuable information about the slug microbiome for potential integrated pest research applications.
