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.     

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.     

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.     

Use of lichen secondary metabolites as antifeedants to protect higher plants from damage caused by slug feeding

Extracts of 15 species of lichen were tested for antifeedant properties against the field slug Deroceras reticulation (Müller) (Mollusca: Pulmonata). All but three showed some activity and two of these were from endolithic species. The most effective extract was from Letharia vulpina. The major active compound from this species, vulpinic acid, was tested for dose response, applied as a foliar spray to turnip plants and as a dressing to wheat seeds in laboratory experiments. It provided effective protection against slug feeding under these conditions.     

Spatial sampling to detect slug abundance in an arable field

Overuse of molluscicides by farmers in arable systems can lead to environmental and product contamination. Here we assess a simple and inexpensive surface trapping method for monitoring populations of slugs (Deroceras reticulatum and Arion intermedius). This method was biased against small slugs, and against A. intermedius, when compared to direct soil sampling. Regression was used to model the relationship between the results of surface trapping and soil sampling methods. Spatial Analysis by Distance IndicEs (SADIE) algorithms were used to describe the spatial relationships between the two sets of samples. Using both traditional statistical methods and spatial statistics, the spatial information collected from surface traps was sufficient to identify patches and gaps in slug numbers and possibly to allow the spot application of slug control, and thus provide land managers who experience slug damage with a way of reducing molluscicides use, whilst maintaining slug control. Further improvements and applications of the model are discussed.     

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.     

Attractiveness of sown wildflower strips to flower-visiting insects depends on seed mixture and establishment success

Establishing wildflower strips has been suggested as an effective measure to promote pollination services, pest control or general insect biodiversity, but little is known about the integration of these different objectives when selecting flower seed mixtures. In ten agricultural landscapes in the Netherlands, we established a wildflower strip (0.4 – 4.9 ha) with half of each strip sown with a mixture targeting longer-tongued pollinators and the other half sown with a mixture targeting shorter-tongued pollinators and natural enemies. We determined establishment success of sown wildflowers and evaluated the attractiveness of the established flower communities to multiple functional groups of flower visitors: bumblebees (long-tongued pollinators), hoverflies (short-tongued pollinators and natural enemies), and butterflies and total flower-visitor richness (indicators of wider biodiversity values). Bumblebees clearly preferred the pollinator-targeted seed mixture and were positively associated with cover of Fabaceae and negatively with Apiaceae. Hoverflies consistently preferred the natural enemy mixture and were positively associated with Apiaceae. The other target groups displayed no clear responses to seed mixture type but instead were associated with local flower richness within strips. Across sites, responses of flower-visitors to sown mixture types did not depend on wildflower strip size, proportion of surrounding semi-natural habitat, or flower variables. However, all flower-visitors except butterflies increased with increasing established cover or richness of (sown) flower species across sites. Our results suggest that, although species-rich wildflower strips may benefit several species groups, maximising different objectives involves trade-offs between functional groups that prefer short- or long-corolla flowers. Furthermore, our study suggests that sowing a wildflower mixture does not necessarily result in a vegetation with the same composition as the seed mixture as species may establish poorly or not at all. Selection of flower species for seed mixtures should therefore, in addition to insect target group, take the establishment characteristics of plant species into account.     

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.     

Crop monitoring to assess the risk of slug damage to winter wheat in the United Kingdom

The percentage of winter wheat seeds killed by slugs was measured, together with various risk factors, at 93 sites throughout the UK from 1987 to 1990. Estimates of slug populations at each site were obtained from traps baited with methiocarb pellets. The peak number of slugs trapped during the period from July until just before cultivation accounted for 26% of the variability in seed damage, more than any other single risk factor. A combined function of the number of slugs trapped at drilling and the percentage of fine soil aggregates in the seed-bed accounted for 21% of the variability in seed damage. Both (i) the peak number of slugs trapped before drilling, and (ii) the combined function of number of slugs trapped at drilling and the percentage of fine soil aggregates in the seed-bed, have potential for identifying fields with a negligible risk of slug damage to wheat seeds. However, further research is needed to improve the accuracy of forecasting slug damage. In particular, other forms of trap should be tested for their potential use in providing more accurate estimates of slug numbers and biomass at drilling, and techniques of assessing seed-bed conditions should be improved. The percentage of seedlings grazed by slugs was correlated with the numbers of slugs trapped before drilling, at drilling and after crop emergence.     

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.     

Effect of flower traits and hosts on the abundance of parasitoids in perennial multiple species wildflower strips sown within oilseed rape (<Emphasis Type="Italic">Brassica napus</Emphasis>) crops

Reducing the use of insecticides is an important issue for agriculture today. Sowing wildflower strips along field margins or within crops represents a promising tool to support natural enemy populations in agricultural landscapes and, thus, enhance conservation biological control. However, it is important to sow appropriate flower species that attract natural enemies efficiently. The presence of prey and hosts may also guide natural enemies to wildflower strips, potentially preventing them from migrating into adjacent crops. Here, we assessed how seven flower traits, along with the abundance of pollen beetles (Meligethes spp., Coleoptera: Nitidulidae) and true weevils (Ceutorhynchus spp., Coleoptera: Curculionidae), affect the density of parasitoids of these two coleopterans in wildflower strips sown in an oilseed rape field in Gembloux (Belgium). Only flower traits, not host (i.e. pollen beetles and true weevils) abundance, significantly affected the density of parasitoids. Flower colour, ultraviolet reflectance and nectar availability were the main drivers affecting parasitoids. These results demonstrate how parasitoids of oilseed rape pests react to flower cues under field conditions. Similar analyses on the pests and natural enemies of other crops are expected to help to develop perennial flower mixtures able to enhance biological control throughout a rotation system.     

A method to study slug predation on seedlings in the field

Dandelion is a common Asteraceae species that populates disturbed sites and gaps within swards where it becomes an important competitor of grasses. The natural control against dandelion includes seedling predation, with slugs, particularly Arion lusitanicus, being the most important in the Czech Republic. However, the study of slug seedling consumption is difficult because naturally established seedlings are not always available. Therefore, we developed a method of exposing laboratory‐grown seedlings as bait for slug predation. Dandelion seeds were sown in plastic cups containing a bottom layer of moist substrate. The emerged seedlings were thinned to 20 and displayed in an open area. During 2008–2010, the seedling baits were placed at 15 sites at 1 month intervals throughout the dandelion vegetative season, in parallel with plasticine baits that monitored slug feeding activity. For each 1 month interval, seedling survival was observed for a period of 8 days, and the estimated time to death was calculated; the percentage of surviving seedlings was then recorded. This method of seedling presentation demonstrated that local and temporal variation in seedling survival is correlated with slug feeding activity. The advantage of this technique is that the seedlings in baits may be presented at any place and time, as required by the experimental design; however, we found that the estimated time to seedling death was shorter for the exposed baits than for the naturally established seedlings. The method is suitable for the study of plant species other than dandelion, and also for aims other than the study of spatiotemporal trends in seedling consumption by slugs.     

The potential of crop management practices to reduce pollen beetle damage in oilseed rape

A major problem associated with agricultural intensification over recent decades has been the development of insecticide resistance in crop pest populations. This has been a particular issue for control of the pollen beetle (Brassicogethes aeneus syn. Meligethes aeneus), a major pest of oilseed rape throughout Europe. Sustained and often prophylactic use of pyrethroid insecticides has led to the development of insecticide-resistant beetle populations, and alternatively, more environmentally benign integrated pest management strategies are sought for the pest. The population dynamics of pollen beetles and their natural enemies, and the damage caused by the pest, are influenced by processes acting at multiple scales, from the regional or landscape scale down to the local field or within-field scale. In this review, we focus on the within-field scale, and how crop management factors, including tillage, crop plant density, crop nutrition and crop rotations may be optimised and incorporated into integrated pest management strategies for more sustainable and effective control of the pest.     

The germination and emergence of seeds of winter oilseed rape stored and sown in admixture with pelleted methiocarb

The possibility that pellets of the molluscicide Draza (a.i. methiocarb) might reduce field emergence of seeds of winter oilseed rape (Brassica napus, cv. Jet Neuf) when sown admixed, laboratory germination when stored admixed, or field emergence when both stored and sown admixed was the subject of three separate investigations. Admixture at sowing did not influence the emergence of five seed lots (P > 0·05). Neither did admixture influence loss in germination or change in moisture content during 2 months' storage of one lot in four different regimes (P > 0·05). Field emergence following 2 months' storage in paper bags was not influenced by admixture (P > 0·05), whereas a 12% reduction in field emergence resulting from storage in admixture within polyethylene bags was detected (P < 0·05). Thus short-term storage within paper sacks of winter oilseed rape seeds in admixture with slug pellets containing methiocarb did not damage the seeds. The emergence of five seed lots differed considerably within and between field sowings. Tentative advice on the calculation of sowing rates for different seed lots of winter oilseed rape is provided to account for this variation.     

Effect of seed depth on slug damage to winter wheat

In a field experiment drilled at two depths on three dates in autumn 1988, with or without methiocarb pellets broadcast on the soil surface immediately after drilling, 26% of seeds of winter wheat sown at c. 20 mm depth were killed by slugs compared with only 9% of seeds sown at c. 40 mm. The protection from slug damage provided by this additional 20 mm of depth was comparable with that provided by methiocarb pellets. The effects of seed depth and pellet application did not interact and were consistent on all drilling dates. Thus, fewest seeds and seedlings were killed where methiocarb pellets were broadcast on a seed-bed with seeds sown at 40 mm depth. Intermediate damage was recorded where seeds were sown at 40 mm depth without pellets, or where pellets were broadcast on seeds sown at 20 mm depth. Most seeds and seedlings were killed where seeds were sown at 20 mm depth without pellets. Sublethal damage to seedlings was not affected by sowing depth but was reduced where pellets were broadcast immediately after sowing.     

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.