Low temperature survival in different life stages of the Iberian slug, Arion lusitanicus

The slug Arion lusitanicus Mabille (Gastropoda: Pulmonata: Arionidae) is an invasive species which has spread to most parts of Europe. The area of origin is unknown, but A. lusitanicus seems to cope well with the local conditions in the countries to which it has migrated. It spreads rapidly, occurs often in high densities and has become a serious pest in most European countries. Therefore there is an urgent need for better knowledge of the ecophysiology of A. lusitanicus, such as the influence of climatic conditions, in order to develop prognostic models and strategies for novel pest management practises.The aim of our study was to investigate the influence of subzero temperatures in relation to winter survival. A. lusitanicus is shown to be freeze-tolerant in some life stages. Most juveniles and some adult slugs survived being frozen at −1.3 °C for 3 days, but none of the slugs survived freezing at −3 °C. The eggs survived subzero temperatures (down to −2 °C) probably by supercooling. Juveniles and adults may also survive in a supercooled state (down to −3 °C) but are generally poor supercoolers. Therefore, the winter survival of A. lusitanicus depends to a high degree on migration to habitats protected from low winter temperatures, e.g. under plant litter, buried in the soil or in compost heaps.     

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.     

The influence of temperature on life history traits in the Iberian slug,Arion lusitanicus

The slug Arion lusitanicus is an invasive species which has recently become established in many European countries and is considered a serious pest, both in agriculture and private gardens. The effect of temperature on growth rate, survival, egg developmental time and hatchability of the slug are reported. The growth rate was positively correlated with temperatures up to 20°C and A. lusitanicus continued (on average) to grow until they die. A model describing how growth depends on temperature was developed, and a field survey found that the predicted growth matched the observed with reasonable accuracy. This study confirms the assumption that A. lusitanicus die after egg laying. Free‐ranging A. lusitanicus has an annual life cycle, but our data show that slugs also possess the ability to live for up to 3 years. The egg developmental time was, like growth, positively correlated with temperature and was shortest at 20°C, but the optimum temperature for egg development, when regarded as the temperature with highest hatchability was found to be 10°C. In conclusion, this study has shown that growth and the life‐history traits, egg developmental time and hatchability, of A. lusitanicus are highly influenced by temperature. However, data also show that temperatures within the range 2–20°C did not influence survival rates to any large degree, and that A. lusitanicus can quickly adjust to changes in temperature. The study provides a number of basic parameters which contribute to the understanding of the population dynamics of A. lusitanicus.     

The palatability of 78 wildflower strip plants to the slug Arion lusitanicus

As Arion lusitanicus has been observed in high densities in wildflower strips, the palatability of the foliage of 78 species of sown and naturally occurring plants found in such strips was investigated. In the laboratory, the slugs were offered a surplus of fresh, mature leaves and, after 16 h, a consumption index was calculated to rank the plants according to their palatability to the slugs. Arion lusitanicus showed clear preferences for particular plant species, but more than two thirds of all plants investigated were scarcely eaten. Brassica napus was most eaten, followed by Papaver rhoeas, Capsella bursa-pastoris and Lamium purpureum. Overall, A. lusitanicus preferred sown species to naturally occurring ones and preferred annuals to perennials.     

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.     

The role of glucosinolates and the jasmonic acid pathway in resistance of Arabidopsis thaliana against molluscan herbivores

Although slugs and snails play important roles in terrestrial ecosystems and cause considerable damage on a variety of crop plants, knowledge about the mechanisms of plant immunity to molluscs is limited. We found slugs to be natural herbivores of Arabidopsis thaliana and therefore investigated possible resistance mechanisms of this species against several molluscan herbivores. Treating wounded leaves with the mucus residue (‘slime trail’) of the Spanish slug Arion lusitanicus increased wound‐induced jasmonate levels, suggesting the presence of defence elicitors in the mucus. Plants deficient in jasmonate biosynthesis and signalling suffered more damage by molluscan herbivores in the laboratory and in the field, demonstrating that JA‐mediated defences protect A. thaliana against slugs and snails. Furthermore, experiments using A. thaliana mutants with altered levels of specific glucosinolate classes revealed the importance of aliphatic glucosinolates in defending leaves and reproductive structures against molluscs. The presence in mollusc faeces of known and novel metabolites arising from glutathione conjugation with glucosinolate hydrolysis products suggests that molluscan herbivores actively detoxify glucosinolates. Higher levels of aliphatic glucosinolates were found in plants during the night compared to the day, which correlated well with the nocturnal activity rhythms of slugs and snails. Our data highlight the function of well‐known antiherbivore defence pathways in resistance against slugs and snails and suggest an important role for the diurnal regulation of defence metabolites against nocturnal molluscan herbivores.     

The influence of weather upon the activity of slugs

Summary The activity of slugs was measured by a catch per unit effort sampling system based upon night searching, and was related to the microclimatological conditions in the habitat by regression analysis. The activity of Arion hortensis Fér., Arion subfuscus (Drap.), Arion lusitanicus Mab., Milax budapestensis (Hazay), and of all slugs irrespective of species, was found to be best related to temperature and vapour pressure deficit. The relevance of these results to the application of effective methods for the control of slugs is discussed.     

Feeding deterrent effect of carvone, a compound from caraway seeds, on the slug Arion lusitanicus

The feeding deterrent effect of carvone on the slug Arion lusitanicus was investigated. Carvone, a natural compound from caraway seeds, was incorporated into mulch to reduce its inherent volatility. In a laboratory choice experiment, boxes were filled on one side with carvone‐treated mulch and on the other side with untreated mulch. At carvone concentrations ranging from 0.03–0.75 ml litre^?1 mulch, slugs ate significantly more lettuce on the untreated side. In a laboratory based no‐choice experiment, carvone concentrations of 0.25 and 0.75 ml litre^?1 mulch significantly reduced slug feeding in comparison with the untreated control. Moreover at the highest concentration of carvone (0.75 ml litre^?1 mulch) 50% mortality was recorded over a period of 5 days, indicating a clear molluscicidal effect. Due to its volatility carvone did not decrease plant defoliation by A. lusitanicus when applied directly onto lettuce. Subsequent field evaluation showed 0.75 ml litre^?1 mulch to partially reduce slug feeding damage. However, this effect was not sufficient to significantly increase lettuce yield. The incorporation of a higher carvone concentration into mulch is still to be tested to confirm whether carvone‐treated mulch can be recommended as an effective alternative approach to chemical slug control.     

Cold tolerance and freeze-induced glucose accumulation in three terrestrial slugs

Cold tolerance and metabolic responses to freezing of three slug species common in Scandinavia (Arion ater, Arion rufus and Arion lusitanicus) are reported. Autumn collected slugs were cold acclimated in the laboratory and subjected to freezing conditions simulating likely winter temperatures in their habitat. Slugs spontaneously froze at about − 4 °C when cooled under dry conditions, but freezing of body fluids was readily induced at − 1 °C when in contact with external ice crystals. All three species survived freezing for 2 days at − 1 °C, and some A. rufus and A. lusitanicus also survived freezing at − 2 °C. ¹H NMR spectroscopy revealed that freezing of body fluids resulted in accumulation of lactate, succinate and glucose. Accumulation of lactate and succinate indicates that ATP production occurred via fermentative pathways, which is likely a result of oxygen depletion in frozen tissues. Glucose increased from about 6 to 22 μg/mg dry tissue upon freezing in A. rufus, but less so in A. ater and A. lusitanicus. Glucose may thus act as a cryoprotectant in these slugs, although the concentrations are not as high as reported for other freeze tolerant invertebrates.     

Daily activity of the pest slug Arion lusitanicus under laboratory conditions

The daily activity of the slug Arion lusitanicus was studied using time‐lapse video analysis in the laboratory. Under constant temperature (18°C) and 16–h photoperiod, the activity of slugs was measured in half‐hourly periods as locomotor activity, feeding or resting. Track lengths were determined using image analysis. Locomotion of A. lusitanicus was greatest at 5:30, 1.5 h after sunrise, and at 20:30, 1 h after sunset; least locomotor activity occurred between 13:00 and 14:00. The mean distance travelled by A. lusitanicus in 24 h was 10.8 m. The largest slug was the most active and the smallest the least. Slugs spent 68% of 24 hours resting, mainly under artificial shelter traps, 27% in locomotion and 4% feeding. Feeding occurred mainly during the hours of dakness (76%). All categories of behaviour investigated varied greatly between individuals and also between times of day. Homing to artificial shelters and other roost sites was regularly observed within 24 h (41%), but decreased considerably thereafter. The behavioural patterns proved to be in agreement with those found in a previous field investigation and are therefore also discussed with a view to their importance in pest control.     

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.     

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.     

Diversity protects plant communities against generalist molluscan herbivores

Wildflower strips are used to increase natural enemies of crop pests and to conserve insect diversity on farmland. Mollusks, especially slugs, can affect the vegetation development in these strips considerably. Although recent theoretical work suggests that more diverse plant communities will exhibit greater resistance against herbivore pressure, empirical studies are scarce. We conducted a semi‐natural experiment in wildflower strips, manipulating trophic structure (reduction in herbivorous mollusks and reduction in major predators) and plant diversity (2, 6, 12, 20 and 24 sown species). This design allowed us to assess the effect of plant diversity, biomass and composition on mollusks, and vice versa, the effect of mollusc abundance on vegetation. Seven species of mollusks were found in the strips, with the slugs Arion lusitanicus, Deroceras reticulatum and Deroceras panormitanum being most frequent. We found a negative relationship between plant diversity and mollusk abundance, which was due predominantly to a decrease in the agricultural pest species A. lusitanicus. These results are consistent with the hypothesis that plant diversity can reduce the impact of herbivores. However, plant identity also had an effect on mollusks, and accounted for a much larger fraction of the variation in mollusk communities than biodiversity effects. While overall plant diversity decreased during the 3 years of the study, in the final year the highest plant diversity was found in the plots where mollusk populations were experimentally reduced. We conclude that selective feeding by generalist herbivores leads to changes in plant community composition and hence reduced plant diversity. Our results highlight the importance of plant biodiversity as protection against generalist herbivores, which if abundant can in the long term negatively impact plant diversity, driving the system along a “low plant diversity – high mollusk abundance” trajectory.     

Drought tolerance in eggs and juveniles of the Iberian slug, <Emphasis Type="Italic">Arion lusitanicus</Emphasis>

The spread of invasive species is an increasing problem world wide. The invasive slug Arion lusitanicus has spread to most parts of Europe, where it often is considered as a serious pest. There is a need for better knowledge of its ecophysiology to be able to predict the effect of climatic factors, such as temperature and humidity on the population dynamics and abundance. The aim of the present study was to assemble data on the water balance and drought tolerance of eggs and juveniles of A. lusitanicus. Both eggs and juveniles had little capacity to prevent evaporative water loss and lost water when the ambient humidity fell below 99.8 and 99.5%, respectively. The water conductance of the cuticle of juveniles was 242 μg cm⁻² h⁻¹ mmHg⁻¹ and resembles that of other slug species. Both eggs and juveniles of A. lusitanicus tolerate a substantial water loss. There was no difference in water loss resistance between eggs and juveniles, but the eggs were slightly more tolerant to water loss than the juveniles. The percent water loss causing 50% mortality was 72% for the juveniles and 81% for the eggs. Despite A. lusitanicus’ tolerance of substantial water loss, its survival depends on humid habitats.     

Great Spotted Cuckoo Nestlings but not Magpie Nestlings Starve in Experimental Age‐Matched Broods

Nestlings of non‐evicting avian brood‐parasites have to compete for food with foster parents' own nestlings. The outcome of these competitive contests is determined mainly by body size differences between parasitic and host nestlings. As part of the coevolutionary arms race between brood parasites and their hosts at the nestling stage, it has been reported that some host foster parents discriminate against parasitic chicks and are reluctant to feed them. Here, by experimentally creating size‐matched broods of different composition (only magpie Pica pica chicks, only great spotted cuckoo Clamator glandarius chicks or mixed broods), we show that great spotted cuckoo chicks starved in 20.2 per cent (17 of 84) of the parasitized magpie nests even in absence of size asymmetries, while in none (0 of 72) of the nests a magpie chick starved. As far as we know, this is the first record of non‐evictor brood parasitic nestlings starving without being smaller than their host nestmates in a frequently used host species. Nest composition had no effect on chick starvation. The cuckoo nestling starved even in two of the nests occupied by only one cuckoo chick. Our results could be explained by (1) magpies being reluctant to feed cuckoo chicks; (2) parasitic chicks receiving lower‐quality food items or cuckoo nestlings being sensitive to some particular component of the diet (e.g. cereal grains); and (3) the existence of cuckoo chick discrimination ability by magpie foster parents.     

The Larva and Pupa of Pseudoneureclipsis lusitanicus Malicky, 1980 (Trichoptera: Hydropsychoidea): Description,Ecological Data and Taxonomical Considerations

Pseudoneureclipsis lusitanicus Malicky, 1980, is reported from a large tributary of the Loire River, the first record of this genus and species from France. In Europe, this genus was previously known from Portugal. Larval and pupal characters suggest that the genus does not belong to the family Polycentropodidae, as currently classified.     

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.     

Effects of plant extracts on the feeding behaviour of the slug Arion lusitanicus

Methanol extracts of the plants Geranium robertianum, Lepidium sativum, Origanum vulgare, Salvia officinalis, Salvia pratensis, Saponaha officinalis, Thymus vulgaris, Trifolium repens and Valerianella locusta were produced and applied to cotyledons of 6–8 days old rape seedlings to investigate whether they can influence the feeding of the slug Arion lusitanicus on young rape. All plant extracts appeared to reduce slug feeding on rape to some extent, but only the extracts of Saponaria officinalis and V. locusta significantly deterred A. lusitanicus from feeding. The small effects of some extracts may be due to a poor extraction efficiency or an insufficient feeding inhibition capacity of these extracts.     

Spatial distribution and home-range of the pest slug Arion lusitanicus (Mollusca: Pulmonata)

The density and distribution of egg-batches, juveniles and adult Arion lusitanicus, as well as individual home-ranges, were investigated over two seasons. The study was performed on grassland which was mown twice a year and received no herbicides or pesticides, with neighbouring field and stream-side vegetation. Female-mature slugs preferred restricted areas closely neighbouring the taller vegetation of the stream-side vegetation and field, but less-favourable parts of the site were also inhabited in the second year when population densities increased and weather conditions were more favourable. It was postulated that slugs could have home-ranges, as homing behaviour is a well-known phenomenon. The application of a long-lasting individual marking technique enabled calculations of home-ranges (convex polygons) for slugs for the first time. Home-range size averaged 45.4 m² when the population density was low in 1995, and was found to be negatively correlated with density, as it decreased to 12.4 m² in 1996, when population density was high. Mating sites were found to be distinctly closer to the geometric centres of activity than the sites used for egg-deposition. Egg-batches were aggregated under the shelter traps (50 × 50 cm squares of hardboard covered with polystyrene) and the pattern of distribution of egg-batches persisted in the young hatchlings. A number of foreign A. lusitanicus were introduced into the unfavourable centre of the site, and by two to four weeks after release their distribution exactly resembled that of the local ones. In all the various aspects of behaviour investigated, large individual differences were found, suggesting a great plasticity in this generalist species. The importance of the species‘ dispersal capacity in relation to general ecological and applied aspects of control is discussed in the context of the present findings.