Influences of preceding cover crops on slug damage and biological control using Phasmarhabditis hermaphrodita

In a replicated field experiment, ryegrass, vetch and red clover were grown or the soil was kept bare over a 2–month period in summer to compare the effects of these treatments on slug damage to the following crop (Chinese cabbage) and on the efficacy of nematodes (Phasmarhabditis hermaphrodita) applied as biological control agents to the soil at planting time to protect this crop. Slug damage was significantly (c. two times) greater after red clover or vetch than after ryegrass. Damage on plots without cover crop was intermediate and not significantly different from either extreme. Slug damage was reduced by about one‐third by the nematode treatment. The preceding cover crop did not influence nematode efficacy. Numbers of slugs on harvested plants (mainly Deroceras reticulatum and Deroceras panormitanum) were influenced by an interaction between cover crop and nematode treatment. On subplots without nematodes, more slugs were recorded with than without a preceding cover crop. No such differences were found on nematode‐treated subplots. Soil samples were collected at intervals from 0–99 days after nematode treatment to monitor nematode survival and infectivity in bioassays with D. reticulatum. No significant effects of cover crops were detected in bioassays. Moreover, there were no significant effects of nematodes on slug survival. Their effects on slug food consumption were mostly insignificant and any effects were transient and not consistent. However, significantly more slug cadavers contained nematodes when slugs were exposed to nematode‐treated soil. The implications of these results are discussed.     

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.     

Selective grazing of acyanogenic white clover: Variation in behaviour among populations of the slug Deroceras reticulatum

Summary Collections of the slug Deroceras reticulatum were made from grassland sites containing contrasting frequencies of the cyanogenic morph of white clover, Trifolium repens. In choice chamber experiments, slugs obtained from sites with a low frequency of cyanogenic clover showed a significantly greater degree of selective eating of acyanogenic morphs than slugs taken from a site containing a high frequency of cyanogenic clover. Differences in selectivity between populations were caused both by differences in the rate of initiation of feeding on cyanogenic morphs, and by differences in the extent of damage once feeding had been initiated. The implications of these results for the cyanogenic polymorphism of T. repens are discussed.     

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.     

Predation by the Carabid Beetles Pterostichus melanarius and Poecilus cupreus on Slugs and Slug Eggs

Predation on slugs, Arion lusitanicus (Mabille) and Deroceras reticulatum (Müller), and their eggs by the carabid beetles Pterostichus melanarius (Illiger) and Poecilus cupreus (L.) was investigated in the laboratory. Slugs of different size and slug eggs were offered to the beetles in petri dishes with and without several alternative prey. Pterostichus melanarius destroyed eggs of D. reticulatum and A. lusitanicus, with a clear preference for D. reticulatum eggs. The availability of some alternative prey types adversely affected feeding on D. reticulatum eggs by P. cupreus and feeding on A. lusitanicus eggs by P. melanarius. Yet consumption of D. reticulatum eggs by P. melanarius was not significantly influenced by any alternative prey. Only P. melanarius killed small D. reticulatum in the presence of alternative prey. This suggests that P. melanarius and P. cupreus may have the potential to reduce slug populations in the field by destroying slug eggs and, in the case of P. melanarius, killing freshly hatched slugs.     

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.     

Damage to oilseed rape seedlings by the field slug Deroceras reticulatum in relation to glucosinolate concentration

Seedlings of nine commercial cultivars of oilseed rape were exposed to the field slug Deroceras reticulatum immediately after sowing in compost in trays. There was a small reduction in seedling numbers in the presence of slugs which was not related to glucosinolate concentration in seeds or seedlings. However, the number and leaf-area of seedlings with damage symptoms were strongly and inversely related to the total concentration of glucosinolates in seeds and one wk-old seedlings. The presence of barley seedlings as alternative food did not significantly affect this relationship. The glucosinolate concentration of seeds was closely correlated with that of wk-old seedlings. Analysis of individual glucosinolates in four cultivars spanning the range of concentrations found, showed that the concentration of most components declined as total glucosinolate concentration decreased. However, 2-phenyl ethyl-glucosinolate (gluconasturtiin) concentration tended to increase in seeds and 3-indolyl methyl-glucosinolate (glucobrassicin) increased in seedlings as total glucosinolate concentration decreased. Damage by slugs was inversely related to the concentration of those glucosinolates which decreased and was positively correlated with the two compounds which increased as total glucosinolate concentration decreased. The results support the hypothesis that glucosinolates in brassicas protect them from polyphagous herbivores, and, in particular, that an important function of glucosinolates in rape seeds is to protect seedlings from slugs. As glucosinolate concentrations of oilseed rape cultivars continue to decline, so the risk of slug damage to seedlings may well increase.     

Biological control of slugs in winter wheat using the rhabditid nematode Phasmarhabditis hermaphrodita

A field experiment on winter wheat in autumn 1991 investigated the effect of the rhabditid nematode, Phasmarhabditis hermaphrodita, applied to soil at five dose rates (10⁸ - 10¹⁰ infective larvae ha^-1) immediately after seed sowing, on slug populations and damage to seeds and seedlings. The nematode was compared with methiocarb pellets broadcast at recommended field rate immediately after drilling and no molluscicide treatment. Slug damage to wheat seeds and seedlings was assessed 6 and 13 wk after drilling. Seedling survival increased and slug grazing damage to seedlings declined linearly with increasing log nematode dose. These two measures of slug damage were combined to give an index of undamaged plant equivalents, which also increased linearly with increasing log nematode dose. ANOVA showed that, after 6 wk, there were significantly more undamaged plant equivalents on plots treated with the two highest nematode doses (3 × 10⁹ and 1 × 10¹⁰ ha^-1) than on untreated plots, but the number of undamaged plant equivalents on methiocarb-treated plots was not significantly greater than that on untreated plots. Slug populations were assessed by refuge trapping and soil sampling. Deroceras reticulatum was the commonest of several species of slugs recorded. During the first 4 wk after sowing, significantly more slugs were found under refuge traps on plots treated with certain doses of P. hermaphrodita than under traps on untreated plots and more showed signs of nematode infection than expected from the prevalence of infection in slugs from soil samples, suggesting that the presence of P. hermaphrodita altered slug behaviour. Application of P. hermaphrodita had no significant impact on numbers or biomass of slugs in soil during a 27 wk period after treatment, except after 5 wk when slug numbers were inversely related to log nematode dose. However, by this time, numbers in soil samples from untreated plots had declined to levels similar to those in plots treated with the highest dose of nematodes. During the first 5 wk after treatment, c. 20% of slugs in soil samples from untreated plots showed symptoms of nematode infection. It is suggested that this represented the background level of infection in the experimental field rather than spread of infection from treated plots. The apparent lack of impact of P. hermaphrodita on slug numbers and biomass in soil suggests that its efficacy in protecting wheat from slug damage was through inhibition of feeding by infected 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.     

Predation by the carabid beetle Harpalus rufipes on the pest slug Deroceras reticulatum in the laboratory

The Harpalini species Harpalus rufipes, as many other generalist carabids, consume a wide variety of prey and it is known to feed on pest slugs such as the grey field slug Deroceras reticulatum, but quantitative data about the predatory activity of H. rufipes on slugs are very scarce. In laboratory experiments, we assessed the capability of male H. rufipes to kill eggs and different‐sized slugs of the pest species D. reticulatum in either the absence or the presence of alternative live prey (dipteran larvae and aphids). We also investigated the preference of H. rufipes for eggs and hatchlings of D. reticulatum in a choice experiment. H. rufipes killed considerable amounts of eggs and small juveniles (≤5.0 mg) of D. reticulatum, both in no‐choice and in choice situations. Medium‐sized juvenile slugs (10–20 mg) were seldom killed only in no‐choice situations, and no large juveniles (50–60 mg) were killed. Dipteran larvae and aphids were killed also in no‐choice and in choice situations. The type of alternative prey presented with slug eggs affected the survival of the eggs to H. rufipes predation. The presence of dipteran larvae as alternative prey did not affect the survival of juvenile slugs. When eggs and small juvenile slugs were offered together, the survivals of both items were similar. The obtained results under laboratory conditions suggest that the generalist predator H. rufipes might realise an important contribution to the control of pest slugs.     

Complementary video and acoustic recordings of foraging by two pest species of slugs on non-toxic and molluscicidal baits

The effects of adding the molluscicides methiocarb and metaldehyde to pelleted foods on the encounter, acceptance, feeding and post-meal stages of the foraging sequence of the slugs Deroceras reticulatum and Arion distinctus have been studied using two complementary laboratory techniques - video and acoustic recordings. Whereas non-feeding slugs encountered wheat grains at random, slugs which fed on wheat grains or pellets encountered them more frequently because of changes in locomotor pattern and olfactory attraction. Slugs would almost always feed on the first pellet they found, regardless of the presence or absence of molluscicide: thereafter they fed on only one pellet in every four encountered. Far fewer slugs accepted wheat grains. Slugs ate much less from pellets containing molluscicide, and meals were more irregular. The relative amounts of non-toxic pellets of various types which were eaten gave no indication of the relative amounts eaten when molluscicide was added. Meal length did not correlate well with meal size on different pellet types because softer pellets were eaten faster. Most Deroceras fed several times on non-toxic pellets or pellets containing methiocarb, although subsequent meals were shorter than the first meal. Most returned to shelters by dawn. In contrast, metaldehydefed slugs were rapidly immobilised; they seldom fed again, moved little, and few regained shelter. Arion were also inhibited after methiocarb meals but Deroceras were not. Arion distinctus moved less, ate less during a meal, and had fewer meals on nontoxic baits than Deroceras reticulatum.     

Feeding Activity and Survival of Slugs,Deroceras reticulatum,Exposed to the Rhabditid Nematode,Phasmarhabditis hermaphrodita: A Model of Dose Response

The slug, Deroceras reticulatum (Stylommatophora: Limacidae), was exposed to different concentrations of infective dauer juveniles of the rhabditid nematode Phasmarhabditis hermaphrodita, in a two-stage bioassay, at 10°C. Slugs were exposed in groups of 10 or 12 to nematodes in plastic boxes filled with soil aggregates for 3 or 5 days and then transferred individually to petri dishes each containing a disk of Chinese cabbage leaf as food. Subsequently, slug food consumption and survival were measured for 10 to 13 days. Models were developed to describe the way that exposure to the nematode caused inhibition of slug feeding followed by death. Both effects were related to nematode concentrations and time after exposure to the nematode. Following exposure to high concentrations (300,000 dauer juveniles per box), slugs were killed rapidly, within a few days after the end of the exposure period. Following exposure to low concentrations of nematodes (7000 or 15,000 per box), substantial numbers of slugs survived until the end of the bioassay, but feeding activity by these slugs was strongly inhibited. It is suggested that inhibition of slug feeding is important for the success of this nematode as a biocontrol agent.     

Size-specific susceptibility of the pest slugs Deroceras reticulatum and Arion lusitanicus to the nematode biocontrol agent Phasmarhabditis hermaphrodita

The nematode Phasmarhabditis hermaphrodita is a commercially available biocontrol agent against slugs. This product is especially interesting for use in organic farming, where products containing metaldehyde or carbamates cannot be used for controlling pest slugs. We investigated the potential of P. hermaphrodita for the control of the pest slugs Deroceras reticulatum and Arion lusitanicus. These two species are the most harmful slug pests in Switzerland. At different times of the year, we collected slug specimens of different weight and assessed their susceptibility to P. hermaphrodita in the laboratory. Batches of five slugs were subjected to five different doses of nematodes plus an untreated control and replicated three times. During six weeks, feeding and survival of the slugs were recorded. D. reticulatum was strongly affected by increasing nematode doses, irrespective of the slugs' body weight. In small specimens of A. lusitanicus, feeding and survival were strongly affected by the nematodes, while larger specimens remained almost unaffected. Because A. lusitanicus has an asynchronous development in Switzerland, it seems difficult to control the entire population with a single nematode application. To what extent nematodes will be used in practice for slug control depends on their effectivity against the pest slugs of major importance, on the longevity of the molluscicidal effect and on the price of nematodes.     

Effects of metaldehyde and methiocarb on feeding preferences and survival of a slug predator (Pterostichus melanarius (F.): Carabidae,Pterostichini)

The potential for reducing slug populations in crops through predation by generalist carabid beetles is well documented. However, few studies have considered interactions between biological and chemical control agents of slugs. Laboratory assays supported previous findings that the consumption of metaldehyde by slugs (Deroceras reticulatum) leads to increased duration of feeding bouts by carabid beetles (such as Pterostichini) on sub‐lethally affected individuals. However, a similar effect was not found for Pterostichus melanarius exposed to slugs fed on the other widely applied pelleted molluscicide formulation (methiocarb). Examination of beetle survival after consumption of slugs containing molluscicides demonstrated the strong biocidal properties of methiocarb, whereas metaldehyde consumption (ingested through slug predation) did not differ from control slugs killed by freezing. Beetle avoidance of slugs containing a more toxic molluscicide compound and the interaction between slug mucus production and beetle attack rates are discussed.     

Invasive slugs as under-appreciated obstacles to rare plant restoration: evidence from the Hawaiian Islands

Introduced slugs have invaded many parts of the world where they were recognized as important pests of gardens and agriculture, but we know little about the effects of introduced slugs on rare plants in natural areas. The Hawaiian Islands have no native slugs, but over a dozen introduced slug species are now established. We reviewed Rare Plant Recovery Plans produced by the U.S. Fish and Wildlife Service for Hawaii and found that introduced slugs were specifically mentioned as threats or potential threats to 59 rare plant species (22% of all endangered and threatened plants), based mainly on anecdotal observations by field biologists. We then initiated an experimental field study to assess the impact of slug herbivory on the growth and survival of two endangered plant species (Cyanea superba, and Schidea obovata), one non-endangered native species (Nestegis sandwicensis) and two co-occurring invasive plant species (Psidium cattleianum and Clidemia hirta). In mesic forest on the Island of Oahu, we tracked the fate of outplanted seedlings in replicated 1 m² plots, with and without slug control. Slugs decreased seedling survival of the endangered species by 51%, on average. Slugs did not significantly affect survival of the non-endangered or invasive plant species. Introduced slugs seem to be under-appreciated as a direct cause of plant endangerment. Invasive slugs may also facilitate the success of some invasive plant species by reducing competition with more palatable, native plant competitors. Slug control measures are relatively inexpensive and could facilitate rare plant establishment and population recovery.     

FORAGING BEHAVIOUR OF TERRESTRIAL GASTROPODS: INTEGRATING FIELD AND LABORATORY STUDIES

The foraging range of adult snails, Helix aspersa, has beenstudied using radio-transmitters. Snails did not return to anexact roost site after foraging, but often remained in the foodpatch, or returned only to the general roost area. Time lapse video films of the slug Deroceras reticulatum madeunder infra-red lighting in arenas were analysed for tracklengthsand degree of turning, in order to simulate slug movements inan unbounded situation. The results suggest that many food itemsare found by random encounter. Slugs usually ate the first food item found, but often ignoredfood items encountered later. If food was scarce, the slugsfed almost every time. Electronic recordings of bites on a wheatflour pellet over 24 hours show that feeding is most intensein the first two and a half hours from starting to feed, andlater meals are both shorter and less regular. Starved slugsdiffered from fed slugs principally by taking a second mealshortly after the first. When given a choice of a more preferredfood (maize pellets) and a less preferred food (pea pellets)in different ratios, the slugs appeared to encounter pelletsat random, but they fed more from the preferred pellets unlessthe ratio was 1 maize: 7 pea. Starved slugs ate twice as muchas fed ones.     

Predation by the carabid beetles Pterostichus madidus and Nebria brevicollis is affected by size and condition of the prey slug Deroceras reticulatum

1 Slugs are important pests in many agricultural crops but molluscicides commonly used to control slugs affect non‐target organisms. Encouraging biological control may help to reduce molluscicide use, but the efficiency of potential natural enemies needs to be investigated. 2 Serological tests have shown that certain carabid species consume slugs. These techniques, however, do not distinguish between scavenging and true predation, nor do they provide information on the size or other characteristics of the prey consumed. The study reported here was undertaken to establish whether scavenging of dead slugs might be an important factor contributing to positive serological test results. 3 Both Pterostichus madidus (Fabricius) and Nebria brevicollis (Fabricius) consumed Deroceras reticulatum (Müller) under laboratory conditions. Dead slugs were scavenged in preference to injured or healthy slugs. 4 Only small, live slugs (< 0.11 g) were killed by both beetle species, which may, therefore, be incapable of killing larger slugs. 5 These generalist beetle species appeared unable to overcome the defence mucus produced by slugs. The data suggest that positive serological results from field collected beetles may reflect scavenging rather than predation on live or injured slugs.     

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.     

Slugs: Potential Novel Vectors of Escherichia coli O157

Field and laboratory studies were performed to determine whether slugs could act as novel vectors for pathogen (e.g., Escherichia coli O157) transfer from animal feces to salad vegetables. Escherichia coli O157 was isolated from 0.21% of field slugs from an Aberdeenshire sheep farm. These isolates carried the verocytotoxin genes (vt1 and vt2) and the attaching and effacing gene (eae), suggesting that they are potentially pathogenic to humans. Strain typing using multilocus variable number tandem repeats analysis showed that slug and sheep isolates were indistinguishable. Laboratory experiments using an E. coli mutant resistant to nalidixic acid showed that the ubiquitous slug species Deroceras reticulatum could carry viable E. coli on its external surface for up to 14 days. Slugs that had been fed E. coli shed viable bacteria in their feces with numbers showing a short but statistically significant linear log decline. Further, it was found that E. coli persisted for up to 3 weeks in excreted slug feces, and hence, we conclude that slugs have the potential to act as novel vectors of E. coli O157.     

Predation by polyphagous carabid beetles on eggs of a pest slug: Potential implications of climate change

Harpalus rufipes and Poecilus cupreus are two widespread polyphagous carabids which are known to destroy eggs of the pest slug Deroceras reticulatum in the laboratory. To examine the effect of temperature on the predation of the eggs of D. reticulatum by H. rufipes and P. cupreus, a laboratory experiment with different temperatures and a semi‐field experiment including simulated warming were performed. In both experiments, H. rufipes killed more eggs than P. cupreus, and the predatory activity of the former increased significantly with increasing temperature. To our knowledge, this is the first study on predatory activity of polyphagous carabids on the eggs of a pest slug performed under a climate warming scenario. Results suggest that biological pest control performed by polyphagous carabids such as H. rufipes upon pest slugs may be enhanced under predicted climate warming conditions.