Improving slug baits: the effects of some phagostimulants and molluscicides on ingestion by the slug, Deroceras reticulatum (Miiller) (Pulmonata: Limacidae)

The effects of seven potential phagostimulants and of four molluscicidal compounds on feeding were examined by confining slugs with agar gels containing the chemicals in varying concentrations. Sugars generally increased the amount of gel ingested; sucrose more than glucose, lactose and fructose. Feeding increased with increasing sucrose concentration to a maximum and then fell progressively: the optimum concentration lay between 2.5% and 5%. The sweeteners saccharin and aspartame at concentrations up to 2.5% did not increase feeding. Addition of the molluscicides metaldehyde, methiocarb and ferric acetylacetonate to gels containing 2.5% sucrose progressively reduced feeding at concentrations of 0.001% and above. Metaldehyde reduced ingestion more than methiocarb and ferric acetylacetonate was intermediate. The molluscicidal herbicide Ioxynil deterred feeding completely at concentrations of 0.001%. The implications for slug bait development are discussed.     

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.     

Susceptibility of the eggs of the field slug Deroceras reticulatum to contact with pesticides and substances of biological origin on artificial soil

The toxicity of 14 substances, including a number of pesticides, to the eggs of the pest slug Deroceras reticulatum was determined in laboratory experiments. Eggs were kept in contact with a precisely defined artificial soil to which a range of concentrations of the test substances had been applied. Mortality of the eggs was assessed every 24 h and the median lethal doses (LD₅₀) were determined. The herbicides bromoxynil, ioxynil and pyridate + bromoxynil, the insecticides thiocyclam, diflubenzuron and azadirachtin, the molluscicides metaldehyde and methiocarb, and other compounds such as carvone, iron‐EDDHA, saponin, and an extract of Pongamia pinnata, killed the eggs after periods of exposure ranging from 2 to 14 days, depending on the compound and the dose. Only two compounds, the insecticides imidacloprid and teflubenzuron, failed to kill the eggs of D. reticulatum at any of the doses tested. Values of LD₅₀ below 0.01 mg a.i. cm^?2 were obtained for the herbicides bromoxynil, ioxynil and pyridate + bromoxynil, and for the biological pesticide azadirachtin. The feasibility of slug egg control in different contexts is discussed.     

Evaluation of defined-area trapping for estimating the density of the field slug Deroceras reticulatum (Müller)

A novel quantitative method (defined-area trapping) devised in New Zealand for sampling slugs was tested in pastures in the UK and compared with cold water extraction processes and surface searching. Despite the different soils and conditions compared with New Zealand, the technique gave results for the UK comparable with accepted methods of estimating slug density with savings in time and labour and provided a non-destructive means of sampling for slugs.     

Electrophysiological and pharmacological characteristics of buccal smooth muscle of the pest slug Deroceras reticulatum

Buccal mass muscle of the pest slug Deroceras reticulatum was examined by conventional tension recording and the sucrose-gap electrophysiological technique. Elevated potassium salines induced dose-dependent depolarisations accompanied by tonic contractures with superimposed rapid twitch contractions. The latter were suppressed at over 40 mmol · l⁻¹ external potassium, where depolarisation-induced inactivation of voltage-sensitive calcium channels may have occurred. Acetylcholine caused significant dose-dependent depolarisations and tonic contractures, while 5-hydroxy tryptamine induced lower depolarisations accompanied by phasic contractile activity superimposed on low level tonic force. Of the purines examined only guanosine triphosphate caused significant mechanical activity above a threshold of 0.1 μmol · l⁻¹. The tetrapeptides inhibited buccal muscle spontaneous activity, but the related small cardioactive peptide B was weakly excitatory. The amino acids glutamate and gamma-aminobutyric acid were weakly excitatory on buccal muscle while the molluscicides metaldehyde and methiocarb disrupted normal mechanical activity of the feeding musculature. Acetylcholine and 5-hydroxytryptamine appear to have major roles in regulating feeding muscle activity, seemingly modulated by guanosine triphosphate and inhibited by phenylalanine-methionine-arginine-phenylalanine-NH₂ and phenylalanine-leucine-arginine-phenylalanine-NH₂. Accepted: 22 July 1999     

A bioassay for screening materials influencing feeding in the field slug Deroceras reticulatum (Müller) (Mollusca: Pulmonata)

Test materials were incorporated in wheatflour pellets to measure their effect on slug feeding. The dry weights of individual pellets were measured before and after exposure for 24 h to starved slugs. The method gave consistent results, and can accommodate test materials with different physical properties. The phagostimulant effect of sucrose was confirmed. An extract of the herb tarragon (Artemisia dracunculus) was the most effective antifeedant of the materials used at the concentrations tested. The method is compared with other published techniques.     

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.     

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.     

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 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.     

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.     

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.     

Biochemical and bioassay analysis of resistance of potato (Solanum tuberosum L.) cultivars to attack by the slug Deroceras reticulatum (Muller)

A method is described for using young field slugs Deroceras reticulatum (Muller) in a bioassay study of biochemical resistance of potato (Solanum tuberosum L.) cultivars to slugs. Tuber parts or an artificial diet were provided as food sources. Comparisons were made of feeding, survival and weight gain between the susceptible cultivar Maris Piper and the resistant cultivar Pentland Dell. Biochemical analyses were made of these two cultivars and the resistant cultivars Stormont Enterprise and Majestic. Comparisons of tuber sections and peelings as food sources indicated factors affecting growth were located in the surface layers of the tubers. Phenolics and glycoalkaloids were concentrated in the surface layers but the amounts were similar in the susceptible and resistant cultivars and the bioassays indicated that neither acting alone could explain resistance. The amounts and distribution of free amino acids also did not correlate with resistance although when supplied in the artificial diet they partly inhibited feeding. Proteinaceous inhibitors of slug gut proteolytic enzymes were present throughout the tubers but were not concentrated in the surface layers and the amounts were similar in the different cultivars thus they too did not explain the difference in susceptibility between the cultivars. Bioassays using acetone extracts (low molecular weight substances) and acetone powders (high molecular weight substances) either alone or in combination indicated that the resistant cultivar Pentland Dell contained a high molecular weight substance which together with a low molecular weight substance from either the same cultivar or the susceptible Maris Piper could confer resistance. Bioassays using protein extracts supplied in the presence or absence of chlorogenic acid indicated that this mechanism could comprise enzymic oxidation of phenolics. Assays of phenolase confirmed this since activity was highest in the outer layers of the tubers and was highest in the three resistant cultivars. Thus the chief resistance factor identified was high phenolase activity acting rapidly on phenolics when the slug first bites the tuber surface. The quantity of phenolics per se did not control the resistance. Thus while phenolics must be available, resistance is compatible with low blackening on cutting the tuber.     

The acceptability of meadow plants to the slug Deroceras reticulatum and implications for grassland restoration

Background and Aims

Despite the selective pressure slugs may exert on seedling recruitment there is a lack of information in this context within grassland restoration studies. Selective grazing is influenced by interspecific differences in acceptability. As part of a larger study of how slug–seedling interactions may influence upland hay meadow restoration, an assessment of relative acceptability is made for seedlings of meadow plants to the slug, Deroceras reticulatum.

Methods

Slug feeding damage to seedling monocultures of 23 meadow species and Brassica napus was assessed in microcosms over 14 d. The severity and rate of damage incurred by each plant species was analysed with a generalized additive mixed model. Plant species were then ranked for their relative acceptability.

Key Results

Interspecific variation in relative acceptability suggested seedlings of meadow species form a hierarchy of acceptability to D. reticulatum. The four most acceptable species were Achillea millefolium and the grasses Holcus lanatus, Poa trivialis and Festuca rubra. Trifolium pratense was acceptable to D. reticulatum and was the second highest ranking forb species. The most unacceptable species were mainly forbs associated with the target grassland, and included Geranium sylvaticum, Rumex acetosa, Leontodon hispidus and the grass Anthoxanthum odoratum. A strong positive correlation was found for mean cumulative feeding damage and cumulative seedling mortality at day 14.

Conclusions

Highly unacceptable species to D. reticulatum are unlikely to be selectively grazed by slugs during the seedling recruitment phase, and were predominantly target restoration species. Seedlings of highly acceptable species may be less likely to survive slug herbivory and contribute to seedling recruitment at restoration sites. Selective slug herbivory, influenced by acceptability, may influence community-level processes if seedling recruitment and establishment of key functional species, such as T. pratense is reduced.     

Responses of slug numbers and slug damage to crops in a silvoarable agroforestry landscape

1. Alternative farming practices such as set-aside and agroforestry are likely to be of continuing interest to European agriculture but may have associated problems, such as increased populations of crop pests such as slugs.
2. A silvoarable agroforestry experiment has been in progress since 1987 at Leeds University Farms at Bramham, West Yorkshire, UK. It consists of four replicate blocks, each with rows of trees separating alleys of arable crops; all four blocks have their own arable control areas in adjacent fields.
3. Pitfall trap catches within the experiment indicate that the slug population increased over the period 1991–94. The increase was greatest, and most consistent, within the tree rows in the agroforestry blocks. The increase was slower and less consistent in the arable controls and the arable areas within the agroforestry blocks.
4. In spring 1994, the slugs in each of the treatments in the agroforestry experimental area were sampled using pipe traps, refuge traps and pitfall traps. The number and diversity of slugs were highest in the grassed understorey beneath the rows of trees and significantly higher in the alleys between the rows of trees than in the arable control areas.
5. The levels of slug damage to a pea crop were assessed by surveys that recorded the number of emerging plants and the number of damaged leaves per plant. There were significant correlations between the number of slugs caught and the damage to the crop by slugs. It is concluded that slugs have the potential to be important pests of some crops in silvoarable agroforestry landscapes and that this could influence the choice of crops for this type of farming.
6. Major conclusions are emboldened in the Discussion.     

The importance of temperature and moisture to the egg-laying behaviour of a pest slug, Deroceras reticulatum

Oviposition behaviour is important when modelling the population dynamics of many invertebrates. The numbers of eggs laid are frequently used to describe fecundity, but this measure may differ significantly from realised fecundity. Oviposition has been shown to be important when describing the dynamics of slug populations, which are important agricultural pests. The numbers of eggs laid by Deroceras reticulatum and their viability were measured across a range of 16 temperature (4, 10, 15 and 23°C) by moisture (33%, 42%, 53% and 58% by dry soil weight) experimental combinations. A fitted quadratic response surface model was used to estimate how D. reticulatum adjusted its egg laying to the surrounding temperature and moisture conditions, with most eggs being laid at a combination of 53% soil moisture and 18°C. The number and proportion of viable eggs also covaried with temperature and moisture, suggesting that D. reticulatum may alter their investment in reproduction to maximise their fitness. We have shown that the number of viable eggs differs from the total number of eggs laid by D. reticulatum . Changes in egg viability with temperature and moisture may also be seen in other species and should be considered when modelling populations of egg-laying invertebrates.     

Low Temperatures Suppress Growth of the Ciliate Parasite, Tetrahymena rostrata , and Pathogenicity to Field Slugs, Deroceras reticulatum

The slug parasitic ciliate protozoan, Tetrahymena rostrata , was isolated from the slug Deroceras reticulatum and used in bioassays against D. reticulatum at 10 and 17oC and in in vitro growth experiments at a range of temperatures. The parasite reproduced, and significantly reduced the life span of juvenile D. reticulatum at 17oC, but not at 10oC.     

Susceptibility and immune response of Deroceras reticulatum, Milax gagates and Limax pseudoflavus exposed to the slug parasitic nematode Phasmarhabditis hermaphrodita

We exposed three slug species (Deroceras reticulatum (Müller), Milax gagates (Draparnaud) and Limax pseudoflavus L.) to the parasitic nematode Phasmarhabditis hermaphrodita Schneider. P. hermaphrodita was able to cause mortality and feeding inhibition to both D. reticulatum and M. gagates but did not negatively affect L. pseudoflavus. On dissection of surviving L. pseudoflavus large numbers of P. hermaphrodita were found encapsulated in the shell of the slug. We found that by increasing shell size, the slug was able to trap invading nematodes, which could be an immune response to P. hermaphrodita invasion. This is the first report of a slug defense mechanism to inhibit P. hermaphrodita.