Exotic Slugs Pose a Previously Unrecognized Threat to the Herbaceous Layer in a Midwestern Woodland

Developing effective restoration strategies requires first identifying the underlying factors limiting native plant recovery. The slug Deroceras reticulatum is an important herbivore in Europe, a global agricultural pest, and is introduced and abundant throughout eastern North America, but little information is available on the effect of this exotic herbivore on the forest herbaceous layer. Here, we test the palatability of 12 forest herbs to the introduced slug D. reticulatum and use field surveys to determine the degree to which slugs are damaging plants in the field. In laboratory feeding trials, slugs readily consumed most plants, but avoided the grass Elymus virginicus, the invasive forb Alliaria petiolata (garlic mustard), and thicker leaved plants. In the field, we documented significant slug damage, with close to 50% or more of plant leaves damaged by slugs on five of the six native species tested. Slug damage in the field was predicted by laboratory‐determined acceptability, but was significantly greater on short‐statured rosette species than on erect plants for a given acceptability value. Our results identify introduced slugs as an important, but overlooked obstacle to forest herb restoration and potential drivers of larger scale understory compositional change. The relaxed herbivore pressure on A. petiolata, relative to native competitors, suggests that invasive plant removal alone may not result in the recovery of native flora. Rather, restoration of unpalatable native species should accompany invasive plant control in slug invaded areas. Erect forbs, thick‐leaved plants, and graminoids should have the greatest success where introduced slugs are abundant.     

Plant characters related to slug feeding: a re‐analysis of feeding studies using trait data from botanical databases and literature

Slugs feed on some plant species but not on others for reasons that are not yet fully understood. We re‐examined the two largest studies on the preference of Arion lusitanicus for different plant species. Briner & Frank (1998) measured the consumption index of slugs (CI_B) based on the dry leaf mass eaten per day per gram of slug mass. Kozlowski & Kozlowska (2009) also measured a consumption index of slugs (CI_K) but on the basis of the area eaten per day per gram of slug mass. The two indices showed a moderate positive rank correlation. Briner & Frank (1998) found that slugs preferred annual to perennial plants and crops rather than wild species. On the other hand, Kozlowski & Kozlowska (2009) found no statistically significant difference in slug preference for annuals, biennials or perennials. Using botanical databases we selected plant traits related to slug herbivory and analysed 141 species. We first analysed the two data sets separately and found that CI_B was higher for seedlings with a higher relative growth rate although this result was only marginally statistically significant. In addition, we found that annuals were consumed more than perennials and that cultivated plants were consumed more than wild plants. This is in agreement with the conclusions of Briner & Frank (1998). For CI_K slugs consumed less from plants with high dry matter content (DMC). The use of classification and regression tree models solves the problem of analysing datasets with missing values. Regarding CI_B, the tree models indicated that life cycle was the major branch. Within perennials, cultivated/wild origin of plants was the most important predictor of slug feeding. Within wild perennials slugs ate more from plants with low specific leaf area (SLA), i.e. relatively thick leaves. Within annuals we found the unexpected result that slugs ate more from plant species with either alkaloids or glucosinolates than from species without one of these compounds. For CI_K, the results of tree models showed that slugs preferred shade‐intolerant plants to shade‐tolerant plant species. Within the shade‐tolerant group slugs fed more on leaves with low DMC. We only partially understand which factors make plants acceptable to slugs. We discuss this issue along with the pros and cons of the two methods used to calculate CI.     

Notonomus gravis (Chaudoir) (Coleoptera: Carabidae) predation of Deroceras reticulatum Müller (Gastropoda: Agriolimacidae), an example of fortuitous biological control

The increasing use of pesticides in broad-acre cropping in South eastern Australia is suspected to have reduced native carabid beetle populations which fortuitously control potential pest populations. Slugs are increasingly becoming an establishment pest of canola, which is often attributed to stubble retention introduced to arable farming systems. Exclusion enclosures were employed to test the effect of the native carabid Notonomus gravis on the exotic pest slug Deroceras reticulatum. The native predatory species limited D. reticulatum populations and this was further supported by a negative field association between the predator and slug numbers. However, while N. gravis contributed to control of slug populations, enclosure experiments suggest that slug damage was not reduced below economic thresholds by this predator alone. Although N. gravis provides a “lying in wait” pest control option for slugs, multiple predators and environmental interactions need to be considered in developing robust integrated pest management guidelines.     

Seed consumption and dispersal of ant-dispersed plants by slugs

In beech-dominated forests in Central Europe, many spring geophytes show adaptations to seed dispersal by ants (myrmecochory). Ants, however, can be rare in such moist forests. Motivated by observations of slug feeding on seeds we investigated the seed consumption of two plant species, Anemone nemorosa and Asarum europaeum, by slugs, in a series of experiments. In a seed predation experiment in a beech forest, we found that seed removal was strongly reduced when gastropods were excluded from the seed depots. The contribution of insects, including ants, and rodents to seed removal was relatively less but differed between May and July. In the laboratory, slug species, in particular Arion sp., consumed seeds of both plant species. Slugs either consumed the elaiosomes of seeds or swallowed seeds intact. Swallowed seeds were defecated undamaged and germinated as well as control seeds when buried overwinter, indicating the potential for seed dispersal by slugs. We also recovered seeds of myrmecochores in the faeces of several slugs caught in forests. In a slug release experiment in the forest, slugs moved up to 14.6 m (mean 4.4 m) in 15 h, which is the median gut passage time of seeds based on measurements made in the laboratory. We also found that when slug-defecated seeds were offered to rodents, these were less attractive than control seeds, suggesting that passage through the slug gut reduces seed predation risk. Our results demonstrate that slugs are significant consumers of elaiosomes or entire seeds of ant-dispersed plants and that they can function as seed dispersers of these plants.     

Predation on the slug Deroceras reticulatum by the carabid beetles Pterostichus madidus and Nebria brevicollis in the presence of alternative prey

1 Slugs are important pests in many agricultural crops and potential biological control agents are being studied as an alternative to molluscicides. Carabid beetles may be able to reduce slug populations, but their role as control agents may be influenced by the presence of alternative prey. 2 Attacks on the pest slug Deroceras reticulatum (Müller) by the carabid beetles Pterostichus madidus (Fabricius) and Nebria brevicollis (Fabricius) were investigated in the presence of alternative prey (earthworms and Calliphora fly larvae). Consumption of slug eggs and aphids was also investigated. 3 All five prey types were consumed to varying degrees during the experiments. Both beetle species showed a significant preference for Calliphora larvae over slugs. Pterostichus madidus showed a significant preference for earthworms over slugs. No preference was shown between earthworms or Calliphora larvae by P. madidus females or N. brevicollis. However, P. madidus males showed a significant preference for Calliphora larvae over worms. Pterostichus madidus showed no preference between slug eggs and aphids; N. brevicollis showed a significant preference for aphids over slug eggs. 4 The results from this study indicate that generalist beetles will often attack other prey in preferences to adult slugs. Slugs may not be preferred because of their mucus. Other prey items occur frequently in arable soils and generalist carabids may ignore slugs altogether and may only feed on them when slug density is high or other prey are unavailable.     

Impact of the field slug Deroceras reticulatum on establishment of ryegrass and white clover in mixed swards

The relationship between numbers of Deroceras reticulatum and the establishment of ryegrass cv. Melle and white clover cv. Milkanova was studied on a mini-plot experiment. Assessments 12 and 33 days after sowing showed that Deroceras reticulatum had a proportionally greater impact on survival and growth of clover than on ryegrass. Slugs had no apparent effect on numbers or growth of three species of broad-leaved weeds (Senecio vulgaris, Cardamine hirsuta and Epilobium sp.) which occurred in the field experiment. In pot experiments where seedlings of ryegrass together with one of three clover cultivars, with or without chickweed (Stellaria media), were exposed to Deroceras reticulatum, seedlings of white clover cv. Aran were less affected by slug grazing than cvs S184 or Milkanova. The presence of different clover cultivars did not significantly influence the impact of slugs on growth of ryegrass or chickweed, nor did the presence or absence of chickweed influence the effect of slugs on ryegrass and clover seedlings. Slugs had less impact on the growth of chickweed than on ryegrass or clover. Thus slug grazing would make clover less able to compete with chickweed as well as the other weeds found in the mini-plot experiment.     

Effects of seed passage through slugs on germination

Seed dispersal by invertebrates is mostly external (e.g. by ants). However, internal dispersal (endozoochory) seems to be uncommon due to size limitations. Slugs are generalist herbivores and increasing evidence suggests that they often disperse seeds. Nevertheless, we know very little on the consequences for plant recruitment. Here, we assess the effect of slug seed passage on germination and early seedling establishment of a set of nine common plant species with limited dispersal capabilities (unassisted or ant dispersed). Germination trials were performed under natural conditions (NW of Spain). Size was a clear limitation for seed ingestion: smaller seeds were eaten more readily, whereas only the largest slugs could swallow the largest seeds. All ingested seeds were voided undamaged. Only not-ingested seeds (the biggest) were damaged, with chewing marks in the surface and 0.8% (N = 250) were broken. In some cases, slugs ate the elaiosomes but discarded the seeds. Slug seed passage had an overall positive effect on total germination and sped it up in two species. Elaiosome removal by slugs had also a positive effect in Ulex europaeus seeds (+160%). However, slugs had no effect on early seedling survival and growth of the study species. Our results show that slugs are effective dispersers in terms of seed treatment in the digestive track. However, according to their reduced movement range (in the range of tens of metres; as shown by other studies), they can only provide rather limited dispersal as compared to vertebrate dispersers. This can be nonetheless significant for species with limited dispersal, e.g. unassisted and ant-dispersed plants, for which they act as non-standard dispersers.     

Abundance,species richness and feeding preferences of introduced molluscs in native grasslands of Victoria,Australia

Abstract Introduced molluscs have invaded endangered, remnant native grasslands of south‐eastern Australia, but few studies have investigated their distribution, abundance or potential impact. Molluscs were surveyed in grassland sites across an urban to rural transect west of Melbourne, Australia. It was confirmed that several introduced mollusc species have invaded these areas. Three snail and five slug species were identified, none of which was native to Australia. The most common species was the brown field slug (Deroceras panormitanum). Mollusc capture and species richness were positively related to the degree of urbanization in the surrounding landscape. There was also a negative relationship with fire frequency. Feeding trials revealed selective herbivory by the black‐keeled slug (Milax gagates) among native plants. Anecdotal evidence that variable glycine (Glycine tabacina) and button wrinklewort (Rutidosis leptorrhynchoides) are palatable to molluscs was supported. Mollusc herbivory may potentially lead to reduced fitness of palatable species, and changes in community composition and structure.     

Microbes to-go: slugs as source for Caenorhabditis elegans microbiota acquisition

Research on the Caenorhabditis elegans microbiota only recently started, with little known about how C. elegans acquires its microbiota. Slugs live in the same habitat as C. elegans and are known vectors for the worm. Hence, we wondered how the passage through a slug affects the C. elegans gut microbiota and whether worms can acquire bacteria from the slug. Using fluorescently labelled microbiota and 16S rRNA gene amplicon sequencing, we evaluated microbiota persistence and acquisition in C. elegans after slug passage. We compared C. elegans gut microbiomes isolated from wild-caught slugs to the microbiomes of worms after experimental slug passage to compare similarities and differences in microbiome composition. We found that microbiota persists in C. elegans while passing the slug gut and that worms simultaneously acquire additional bacteria species from the slug. Although the amplicon sequencing variant (ASV) richness of worms from the experiment did not exceed the richness of worms that naturally occur in slugs, we found a high number of shared ASVs indicating the importance of commonly associated microbiota. We demonstrate that C. elegans can take advantage of its passage through the slug by acquiring new potential microbiota without losing its native microbiota.     

Body size and the colonisation of cereal crops by the invasive slug Arion lusitanicus

The invasive slug Arion lusitanicus lives in undisturbed stands of grass or herbaceous plants from where it disperses into crops. Factors that determined the dispersal of slugs from a grassy orchard (O) into an adjacent cereal stand were investigated. Slug‐feeding activity, abundance and body weight were established along a 120 m transect across an orchard and a cereal crop. Slugs in the source population in the orchard were more abundant and lighter in 2008 than 2009. The slugs that left the orchard and moved into the cereal crop were heavier than those that remained in the orchard and the distance they travelled was positively correlated with their weight. The abundance of slugs in the cereal crop decreased with the increase in the distance from the source population, more so in 2008, when slugs were light in weight and accumulated near the edge of the orchard, than in 2009 when the slugs were heavier and distributed more evenly. The feeding activity of the slugs leaving the orchard and distance they dispersed also increased during the course of the season. Long distance dispersal is achieved by crawling, the speed of which increased with slug size. Seasonal and annual variation in body size thus affected the distribution of slugs in the cereal crop and the distance they dispersed.     

Daily activity rhythm and use of shelter in the slugs Deroceras reticulation and Arion distinctus under laboratory conditions

Daily activity of slugs, Deroceras reticulatum and Arion distinctus, was studied in the laboratory in relation to the presence of shelters so as to define optimal conditions for using traps to forecast crop damage. Under constant temperature and humidity, activity of slugs began with the lights off. Its arrest occurred after a period of activity with the lights on. Slugs rested most frequently under a shelter on bare earth and rarely used the same shelter for more than two consecutive days. When food was placed under the shelter, the number of slugs found under the shelter was more constant throughout the 24 h period, but lower during diurnal rest. The presence of 4% methiocarb pellets under the shelter led to an increased occupation by slugs, due to the poisoning of some of them. Acts of aggression were more numerous in A. distinctus than in D. reticulatum. In D. reticulatum the smallest slug was the least aggressive and suffered more attacks from the other slugs. In A. distinctus the numbers of attacks suffered or provoked varied little with the size of the slug, but the smallest slug showed less interactions with other slugs.     

Contrasting predation pressure of different ground beetles on slugs and their eggs

Slugs such as Deroceras reticulatum Müller (Pulmonata: Agriolimacidae) cause crop losses in temperate regions worldwide. Numerous species of ground beetles (Coleoptera: Carabidae) feed on slugs, but possible interactive effects are poorly known. Here, we compared predation pressure on slug eggs and slug immatures among Abax parallelepipedus Piller and Mitterpacher, Pterostichus niger Schaller, and Pterostichus melanarius Illiger. The latter was most effective against slug eggs but least effective against immature slugs compared to the other species, demonstrating some specificity of ground beetle predation on life stages. Slug egg predation of P. niger in combination with both other species was synergistic, with up to twice as many eggs consumed as for single species treatments. The effect of species combinations on immature slugs showed no differences from expectations based on single species treatments. Our results indicate that combinations of ground beetle species are favourable for the suppression of slugs in early life stages.     

Measuring the effects of invasive species on the demography of a rare endemic plant

The impacts of invasive species are among the greatest threats to the persistence of native species and communities. Yet most work on rare plants has focused on issues such as habitat fragmentation and genetic diversity, while few studies have quantified the impacts of invasive plants on native ones or investigated the underlying mechanisms of those impacts. I used removal experiments to assess the effects of invasive grasses on the seedling and adult demography of an endangered California endemic, Oenothera deltoidesssp. howellii. Invasive plant removal significantly increased O. deltoides seedling recruitment, but had no effect on adult plants. Differences in seedling recruitment were primarily driven by greatly increased seedling emergence rates in removal plots, although there was also some evidence of higher seedling survivorship with invasives removal. Differences in habitat type strongly influenced both the effects of removal treatments and O. deltoides demography, with areas that support natural recruitment showing weaker treatment effects and higher overall recruitment, but lower adult survivorship, compared to those under restoration through planting. These results indicate that inhibition of germination due to reduced soil disturbance, rather than resource competition, appears to be the strongest impact of invasive plants on this rare endemic. Although previous work has documented the importance of changed disturbance regimes in generating invasion impacts, invader effects on rare plants are generally presumed to result from resource competition. Studies like this one highlight the need for a greater emphasis on understanding the mechanisms by which invasive plants impact native ones, and the importance of such information in designing conservation and management strategies.     

Contrasting effects of an invasive ant on a native and an invasive plant

When invasive species establish in new environments, they may disrupt existing or create new interactions with resident species. Understanding of the functioning of invaded ecosystems will benefit from careful investigation of resulting species-level interactions. We manipulated ant visitation to compare how invasive ant mutualisms affect two common plants, one native and one invasive, on a sub-tropical Indian Ocean island. Technomyrmex albipes, an introduced species, was the most common and abundant ant visitor to the plants. T. albipes were attracted to extrafloral nectaries on the invasive tree (Leucaena leucocephala) and deterred the plant’s primary herbivore, the Leucaena psyllid (Heteropsylla cubana). Ant exclusion from L. leucocephala resulted in decreased plant growth and seed production by 22% and 35%, respectively. In contrast, on the native shrub (Scaevola taccada), T. albipes frequently tended sap-sucking hemipterans, and ant exclusion resulted in 30% and 23% increases in growth and fruit production, respectively. Stable isotope analysis confirmed the more predacious and herbivorous diets of T. albipes on the invasive and native plants, respectively. Thus the ants’ interactions protect the invasive plant from its main herbivore while also exacerbating the effects of herbivores on the native plant. Ultimately, the negative effects on the native plant and positive effects on the invasive plant may work in concert to facilitate invasion by the invasive plant. Our findings underscore the importance of investigating facilitative interactions in a community context and the multiple and diverse interactions shaping novel ecosystems.     

Soil conditioning effects of Phragmites australis on native wetland plant seedling survival

Interactions between introduced plants and soils they colonize are central to invasive species success in many systems. Belowground biotic and abiotic changes can influence the success of introduced species as well as their native competitors. All plants alter soil properties after colonization but, in the case of many invasive plant species, it is unclear whether the strength and direction of these soil conditioning effects are due to plant traits, plant origin, or local population characteristics and site conditions in the invaded range. Phragmites australis in North America exists as a mix of populations of different evolutionary origin. Populations of endemic native Phragmites australis americanus are declining, while introduced European populations are important wetland invaders. We assessed soil conditioning effects of native and non‐native P. australis populations on early and late seedling survival of native and introduced wetland plants. We further used a soil biocide treatment to assess the role of soil fungi on seedling survival. Survival of seedlings in soils colonized by P. australis was either unaffected or negatively affected; no species showed improved survival in P. australis‐conditioned soils. Population of P. australis was a significant factor explaining the response of seedlings, but origin (native or non‐native) was not a significant factor. Synthesis: Our results highlight the importance of phylogenetic control when assessing impacts of invasive species to avoid conflating general plant traits with mechanisms of invasive success. Both native (noninvasive) and non‐native (invasive) P. australis populations reduced seedling survival of competing plant species. Because soil legacy effects of native and non‐native P. australis are similar, this study suggests that the close phylogenetic relationship between the two populations, and not the invasive status of introduced P. australis, is more relevant to their soil‐mediated impact on other plant species.     

Contagious dispersal of seeds of synchronously fruiting species beneath invasive and native fleshy‐fruited trees

In subtropical Australia, many native and invasive plant species rely on a shared suite of frugivores, largely birds, for seed dispersal. Many native plants fruit during summer in this region, whereas most invasive plants fruit during winter, thus providing the opportunity for contagious dispersal of seeds beneath synchronously fruiting species. We sampled invasive and native seed rain beneath the canopy of a native summer‐fruiting tree Guioa semiglauca and an invasive winter‐fruiting tree Cinnamomum camphora, in three study sites over the course of a year. In July, during peak fruiting season for C. camphora and other invasive species, seed rain of invasive species was higher beneath C. camphora than G. semiglauca. This was partly due to the invasive tree Ligustrum lucidum, whose seed rain was three times higher beneath C. camphora than beneath the native tree. In February, seed rain of native species was more abundant beneath the canopy of G. semiglauca than beneath C. camphora, despite the fact that C. camphora was also fruiting at this time. This was probably due to the larger fruit crop produced by G. semiglauca at this time of year. Our study provides evidence that the presence of invasive bird‐dispersed plants may facilitate contagious seed dispersal of other invaders, and likewise native species may facilitate seed spread of other native plants.     

The Influence of Mucus Production by the Slug,Deroceras reticulatum,on Predation by Pterostichus madidus and Nebria brevicollis (Coleoptera: Carabidae)

Slugs are important pests in many agricultural crops and potential biological control agents are being studied as an alternative to molluscicides. Carabid beetles may be able to reduce slug populations, but the defence mucus of slugs may deter some predator attacks. Interactions between the carabids Pterostichus madidus (Fabricius) and Nebria brevicollis (Fabricius) with healthy and 'stressed' (unable to produce defence mucus) Deroceras reticulatum (Müller) were investigated in laboratory conditions. Both beetle species consumed significantly more stressed slugs than controls. Defence mucus production by control slugs hampered beetle attacks. These generalist beetle species did not direct their attacks at vulnerable parts of the prey as equal numbers of contacts were made on the slug head, mantle and tail. Blowfly ( Calliphora sp.) larvae are readily consumed by P. madidus and N. brevicollis . Calliphora larvae coated in slug defence mucus were less acceptable to both beetle species compared with control larvae. Results indicate that these generalist beetle species are unable to overcome the defence mucus production of healthy slugs. Slugs sub-lethally poisoned by molluscicides may be a more suitable prey item due to a reduction in defence mucus production.     

The effects of crop development upon slug distribution and control by Abax parallelepipedus (Coleoptera: Carabidae)

The polyphagous carabid beetle Abax parallelepipedus has been shown to be capable of controlling slugs within a lettuce crop in previous studies. This report describes experiments undertaken in plots within a polythene tunnel. Field slugs, Deroceras reticulatum, were introduced to plots containing either large or small lettuce plants, at 30 slugs per plot. The plots were further subdivided into those with or without six beetle predators. Slug numbers were assessed after two weeks, and were found to be affected by plant size, both with and without the presence of predators. These two factors had an additive effect, with both small plant size and the presence of beetles causing significant reductions in slug numbers. Plots with beetles contained either males or females, and females were shown to be significantly better at reducing slug numbers than males, particularly within plots of small plants. The four principal treatments (combinations of two plant sizes and the presence/absence of beetles) generated four distinct patterns of slug distribution within the plots. The potential of the residual slug populations to inflict further damage was measured in a subsequent crop of seedling lettuces. It appeared that the beetles were generally incapable of capturing slugs within large lettuce plants, but were effective predators at soil level. Possible reasons for the survival of fewer slugs in plots with small plants, both with and without the presence of predators, are discussed.     

Biofuels and invasive species from an African perspective – a review

A large number of proposed biofuel crops share the same traits as known invasive plant species, many of which are already present in Africa and include species such as Prosopis glandulosa Torrey (Mimosaceae), P. juliflora (Sw.) DC, Leucaena leucocephala (Lam.) de Wit (Mimosaceae), Azadirachta indica A. Juss. (Meliaceae), and others. In this paper, we mainly assess the impacts of invasive Prosopis species in Africa, particularly in Kenya and South Africa. Introduced Prosopis species have invaded over 4 million hectares in Africa, threatening crop and pasture production, reducing underground water reserves, and displacing native plant and animal species. This has major implications for millions of people who depend on natural resources for their survival. It is therefore suggested that known invasive or potentially invasive plant species not be introduced to countries or regions for biofuel production. If (after a stringent cost–benefit analysis) the introduction of a potentially invasive species is deemed critical for economic development and the benefits clearly outweigh the potential costs, countries should endeavour to abide by the Principles and Criteria for Sustainable Biofuel Production developed by the Roundtable on Sustainable Biofuels.