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.     

Effect of predator size and temperature on the predation of Deroceras reticulatum (Muller) (Mollusca) by carabid beetles

Twenty-one carabid species were used in a laboratory study to determine the effect of beetle size and temperature on the predation of one day old Deroceras reticulatum (Muller) slugs. The beetles were caught in arable land at the study site. None of the five small-sized beetle species killed slugs, whereas five of the seven medium-sized beetle species and eight of the nine large-sized beetle species killed slugs. Four of the most abundant beetle species at the study site were used to assess the effect of temperature on the predation of 1-day-old slugs. There were significant differences in the proportion of beetles predating slugs at the different temperatures. Regression analysis showed that there was a significant increase in the proportion of Pterostichus madidus (Fabricius) and Harpalus rufipes (Degeer) beetles predating slugs as temperature increased. Nebria brevicollis (Fabricius) inflicted its highest level of slug mortality at 8°C and its larvae were the only predators to significantly increase slug mortality at 4°C, the lowest experimental temperature. Harpalus aeneus (Fabricius) inflicted significant levels of slug mortality at 20°C, the highest experimental temperature. It appeared that the predatory activity of these beetle species at the five experimental temperatures reflected their annual activity periods in the field.     

Spatiotemporal Analysis of Predation by Carabid Beetles (Carabidae) on Nematode Infected and Uninfected Slugs in the Field

The dynamics of predation on parasites within prey has received relatively little attention despite the profound effects this is likely to have on both prey and parasite numbers and hence on biological control programmes where parasites are employed. The nematode Phasmarhabditis hermaphrodita is a commercially available biological agent against slugs. Predation on these slugs may, at the same time, result in intraguild predation on slug-parasitic nematodes. This study describes, for the first time, predation by carabid beetles on slugs and their nematode parasites on both spatial and temporal scales, using PCR-based methods. The highest nematode infection levels were found in the slugs Deroceras reticulatum and Arion silvaticus. Numbers of infected slugs decreased over time and no infected slugs were found four months after nematode application. The density of the most abundant slug, the invasive Arion vulgaris, was positively related to the activity-density of the carabid beetle, Carabus nemoralis. Predation on slugs was density and size related, with highest predation levels also on A. vulgaris. Predation on A. vulgaris decreased significantly in summer when these slugs were larger than one gram. Predation by C. nemoralis on slugs was opportunistic, without any preferences for specific species. Intraguild predation on the nematodes was low, suggesting that carabid beetles such as C. nemoralis probably do not have a significant impact on the success of biological control using P. hermaphrodita.     

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.     

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.     

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 behaviour and mortality of the slug, Deroceras reticulatum in relation to control with molluscicidal baits containing various combinations of metaldehyde with methiocarb

In terms of control of slug pests, the differing modes of action of the two molluscicides metaldehyde and methiocarb appear to provide some advantages for the former during warm, dry weather and for the latter during cool, wet weather. With a view to exploiting these different modes of action, the feeding behaviour of Deroceras reticulatum (Müller) presented with molluscicidal baits containing various combinations of metaldehyde with methiocarb was investigated. Voluntary feeding trials conducted in the laboratory with both candidate and standard treatments (containing metaldehyde or methiocarb alone) are described. By combining the two active ingredients in certain ratios the total concentration of active ingredients may be reduced without adversely affecting the efficacy of a bait formulation in terms of slug mortality.     

Predation and prey size choice by the carabid beetle Pterostichus melanarius (Coleoptera: Carabidae): the dangers of extrapolating from laboratory to field

The impact of predation by the generalist carabid beetle Pterostichus melanarius (Illiger) on populations of the field slug Deroceras reticulatum (Müller), and the effects of prey size on the predator-prey interaction, were measured under semi-field conditions. It was hypothesized that environmental heterogeneity would lead to very different patterns of comparative mortality than might be deduced from size choice experiments conducted in the laboratory. Results from outdoor mini-plots, emulating conditions in a field of wheat, demonstrated that P. melanarius significantly reduced numbers of slugs from all size classes, with no apparent preferences. This was in marked contrast to results from earlier laboratory studies, where this beetle fed preferentially on the smallest slugs. The slugs in the mini-plots ranged in size from 2-100 mg and the numbers in the mini-plot reflected the size frequency distribution in the field. Beetles in mini-plots containing high densities of slugs increased significantly in weight, in contrast to beetles in mini-plots with low slug density or no added slugs, which did not. Enzyme-linked immunosorbent assays (ELISA), using anti-slug monoclonal antibodies, showed that where there was a higher density of slugs there was more slug protein in the guts of the beetles. It was concluded that environmental heterogeneity probably provided a greater number and diversity of refugia for smaller than for larger slugs, counteracting laboratory-measured size preferences measured in arenas without refugia. These results have implications for a range of ecological studies involving inter- and intra-specific prey size choice, and emphasize the dangers of extrapolating from the laboratory to the field.     

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.     

Differential susceptibility of species of slugs to metaldehyde/bran and to methiocarb baits

Summary Laboratory experiments were designed to study differential susceptibility of nine species of slugs to metaldehyde/bran and to methiocarb baits. Differential susceptibility was found between some of the species for each type of bait, both immediately after baiting and also after a 48 h recovery period. Thus neither type of bait is suitable for use in ecological investigations. This conclusion was supported by evidence that interspecific behavioural interactions occurred when metaldehyde, but not methiocarb, baits were used.At the same time the relative efficiency of the two types of baits as molluscicides was estimated. Methiocarb was shown to be a better molluscicide because, not only did it initially poison more slugs than did metaldehyde, but also a number of the slugs initially poisoned by metaldehyde recovered during the following 48 h period, whereas this did not happen with methiocarb. The similarity between these results and those obtained from field experiments by other workers is discussed.     

Predator interference limits fly egg biological control by a guild of ground-active beetles

We examined whether predator interference could prevent effective conservation biological control of Delia spp. flies, important pests of cole crops, by an assemblage of carabid and staphylinid beetles. In laboratory feeding trials we found that the smaller (<1 cm) beetle species common at our site readily ate dipteran eggs, while the most common large carabid species, Pterostichus melanarius, rarely did. However, P. melanarius did eat several of the smaller beetle species. We conducted two field experiments where we manipulated immigration rates of the ground predator guild and then measured predation on fly eggs. Predation rates were consistently higher in cages where predators were added at ambient densities, compared to cages where ground predators were removed. However, in the second field experiment, when we quadrupled predator immigration rates neither beetle activity-density nor predation rate increased. High immigration rate plots had a higher proportion of P. melanarius in the predator community, compared to plots with beetles added at ambient densities, suggesting that P. melanarius was reducing activity-densities of the smaller beetles, perhaps through intraguild predation. Thus, tactics to improve the biological control of Delia spp. by conserving generalist predators, such as providing in- or extra-field refuges, could be thwarted if the primary predators of fly eggs, small carabids and staphylinids, are the targets of intraguild predation by also-conserved larger predators.     

Tracking predator density dependence and subterranean predation by carabid larvae on slugs using monoclonal antibodies

1. Subterranean carabid larvae are more numerous than surface‐active adults, yet very little is known about their ecological significance, dietary preferences or ability to regulate populations of prey species, particularly pests. Part of the reason for this is that predator–prey interactions beneath the soil are almost impossible to observe. 2. Extensive field studies have shown that adult Pterostichus melanarius (Illiger) can affect the temporal and spatial dynamics of their slug prey. However, if larvae too are feeding on slugs, this could radically affect overall predator–prey dynamics. 3. We tested the hypotheses that P. melanarius larvae would kill and consume two slug species, Deroceras reticulatum Müller and Arion intermedius Normand, under laboratory and semi‐field conditions, and that there would be no significant difference in rates of predation on these slug species. 4. A new monoclonal antibody was developed that was capable of detecting the presence of slug proteins in the guts of P. melanarius larvae. 5. Pterostichus melanarius larvae killed both A. intermedius and D. reticulatum in the laboratory, feeding to a greater extent, and growing more rapidly, on the latter. The larvae were equally effective at reducing numbers of both slug species in a crop of wheat grown in semi‐field mini plots, but predation was affected by density‐dependent intra‐specific competition amongst the beetle larvae. 6. Future modelling of the dynamic interactions between carabids and slugs will need to take into account predation by larvae.     

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.     

The potential of carabid beetles to control slugs in grass/clover swards

Experiments conducted in sward boxes under controlled conditions showed that the carabid beetlesAbax parallelepipedus (Piller &; Mitterpacher) andPterostichus madidus F. controlled slugs in a grass/clover sward. Control was shown to be as good as that by the molluscicide, methiocarb.A. parallelepipedus proved to be more successful thanP. madidus at controlling the slugs, damage to the clover being kept to a minimum.P. madidus controlled the slugs only after some damage to the clover was sustained.     

Detection of scavenged material in the guts of predators using monoclonal antibodies: a significant source of error in measurement of predation?

Molecular detection systems used to analyse the gut contents of invertebrate predators have enhanced our understanding of trophic interactions, but do not distinguish between the methods of consumption. Many predators regularly scavenge, which could have profound implications for quantitative analyses of the dynamics of predation. We report the first quantified assessment of the potential error caused by scavenging in post-mortem measurements of predation in a slug-carabid system. An anti-slug monoclonal antibody was able to detect antigens from decayed slugs after surprisingly long periods, significantly longer on relatively sterile peat than on natural soil. On soil the half-life of antibody-detectable slug proteins was 8.2 days while on peat it was 11.5 days. When slugs that had decayed on soil for 100 h were fed to the carabid predator Pterostichus melanarius, slug proteins could still be identified after 6 h (but not 12 h) digestion. Fresh and decayed slug was eaten in equal quantities by the beetles suggesting no aversion to the latter. The results suggest that significant errors may be caused by scavenging leading to inaccurate interpretation of predation rates in the field.     

The inhibitory effects of the molluscicide metaldehyde on feeding, locomotion and faecal elimination of three pest species of terrestrial slug

Single meals on maize flour pellets containing 0, 0·5, 1, 2, 4, 6, and 8% metaldehyde were analysed in Arion hortensis (agg), Deroceras reticulatum and Deroceras caruanae, by attaching the pellets to a mechanical transducer from which signals were ultimately fed into a BBC microcomputer for on-line analysis. Post-feeding tests were used to investigate toxic effects of metaldehyde and the recovery of slugs was examined daily for 7 days. Bite rates were slightly lower and more irregular on metaldehyde meals especially in A. hortensis. The meal length and number of bites per meal were markedly inhibited by metaldehyde and inversely proportional to the concentration. The size of the bites was also reduced, by about 30%, in meals on 6% pellets compared with 0%. Clear symptoms of poisoning became evident during the meal or normally in the 16-min test period immediately afterwards. In these tests slugs which fed on metaldehyde pellets showed a disruption of their ability to right themselves (after being placed on their side), less activity and a reduced probability of accepting a ‘dummy’ pellet containing no metaldehyde. It is hypothesised that feeding is prematurely terminated primarily because of the toxic effects of the metaldehyde and that aversion also acts to terminate the meal early, by decreasing the probability of continuing to feed as the meal proceeds. At higher concentrations of metaldehyde aversion may be more important than the toxic effects in ending the meal. Faecal elimination is delayed after metaldehyde meals and this contributes to mortality. The estimated lethal doses were about 0·2 mg/g body weight of slug in Deroceras spp. A. hortensis was less susceptible. To increase the likelihood of a lethal dose being ingested the inhibition of feeding needs to be overcome, at least partly, and the results presented indicate the need for a bait formulation which reduces the rate of absorption of the molluscicide from the gut.     

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.     

EFFECTS OF ORALLY AND DERMALLY APPLIED METALDEHYDE ON MUCUS CELLS OF SLUGS (DEROCERAS RETICULATUM) DEPENDING ON TEMPERATURE AND DURATION OF EXPOSURE

Using light and electron microscopy in combination with histochemicaland immunocytochemical techniques, the impact of orally anddermally applied metaldehyde on mucus cells in the digestivetract, the skin, and the salivary gland of the slug Derocerasreticulatum (Müller) was investigated. The studies showedthat metaldehyde induces severe alterations and damages in mycocyteseven under low temperature and humid conditions when sufficientlyhigh doses were applied. After metaldehyde application, notonly the quantity of mucus produced by slugs but also its qualityis modified. Structural, enzymehistochemical and immunocytochemicalinvestigations revealed metaldehyde-induced effects in mucocytesto be related to influences of the molluscicide on serotoninand on energy metabolism. (Received 29 September 1997; accepted 8 December 1997)     

Molecular analysis of predation by carabid beetles (Carabidae) on the invasive Iberian slug Arion lusitanicus

The invasive Iberian slug, Arion lusitanicus, is spreading through Europe and poses a major threat to horticulture and agriculture. Natural enemies, capable of killing A. lusitanicus, may be important to our understanding of its population dynamics in recently invaded regions. We used polymerase chain reaction (PCR) to study predation on A. lusitanicus by carabid beetles in the field. A first multiplex PCR was developed, incorporating species-specific primers, and optimised in order to amplify parts of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene of large Arion slugs, including A. lusitanicus from the gut contents of the predators. A second multiplex PCR, targeting 12S rRNA mtDNA, detected predation on smaller Arion species and the field slug Deroceras reticulatum. Feeding trials were conducted to measure the effects of digestion time on amplicon detectability. The median detection times (the time at which 50% of samples tested positive) for A. lusitanicus and D. reticulatum DNA in the foreguts of Carabus nemoralis were 22 h and 20 h, respectively. Beetle activity-densities were monitored using pitfall traps, and slug densities were estimated using quadrats. Predation rates on slugs in the field by C. nemoralis in spring ranged from 16-39% (beetles positive for slug DNA) and were density dependent, with numbers of beetles testing positive being positively correlated with densities of the respective slug species. Carabus nemoralis was shown to be a potentially important predator of the alien A. lusitanicus in spring and may contribute to conservation biological control.     

Caffeine as a novel toxicant for slugs and snails

In this study, caffeine is shown to act as both a repellent and toxicant against slugs and snails. This research is the first to document the potential of caffeine as a molluscicide. A drench treatment using a 1% or 2% solution of caffeine caused 100% of slugs (Veronicella cubensis) to exit treated soil, and the majority of these slugs subsequently died from caffeine poisoning. A 2% solution of caffeine applied to the growing medium of orchids killed 95% of orchid snails, (Zonitoides arboreus), and gave better control than a liquid metaldehyde product representing the standard commercial control for this pest. Using leaf‐dip bioassays, we discovered that slugs tended to avoid feeding on plant material treated with caffeine solutions 0.1%, and caffeine solutions as low as 0.01% significantly reduced overall feeding by slugs. Due to concerns about chemical residues, available molluscicides generally cannot be applied directly to food crops for control of slug and snail pests. Caffeine is a natural product which is approved as a food additive. Therefore, caffeine may prove useful for protecting food crops from slugs and snails.