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.     

Molecular identification of predation by carabid beetles on exotic and native slugs in a strawberry agroecosystem

Generalist predators have the capacity to exert significant pressure on prey populations. However, integrating them into biological control programs relies on a detailed understanding of their foraging behavior and the levels of trophic connectedness with pest species. Carabid beetles are important predators of slugs, pests of agricultural, floricultural and horticultural crops worldwide, but these interactions have been rarely studied outside the Western Palearctic ecozone. Diagnostic molecular gut-content analysis was used to examine the strength of trophic pathways between a community of carabid beetles and two slug species, the exotic Deroceras reticulatum and native Deroceras laeve, in strawberry agroecosystems. Strawberries were grown according to standard horticultural practices for central Kentucky, following traditional bare ground planting or with the addition of detrital subsidies, to quantify the impact of habitat management on the abundance of pests and the strength of these trophic pathways. Following laboratory characterization of species-specific molecular markers targeting both Deroceras species, carabid beetles collected from a strawberry agroecosystem were screened for slug DNA. Field collections revealed important food web pathways existed between Harpalus pensylvanicus and D. reticulatum, with 7.2% screening positive for these prey yet none screening positive for D. laeve. In contrast, Chlaenius tricolor was found to feed on both slug species in the field, with 16% screening positive for both Deroceras. Despite below normal rainfall limiting slug densities in the field, the results presented here reveal the potential importance of carabid beetles in slug population dynamics in the Nearctic.     

Classical biological control of Aphis gossypii (Homoptera: Aphididae) with Neozygites fresenii (Entomophthorales: Neozygitaceae) in California cotton

In August 1994 and 1995 classical biological control releases were made in cotton in the San Joaquin Valley, California, with an Arkansas strain of the entomopathogenic fungus, Neozygites fresenii, a pathogen of the cotton aphid, Aphis gossypii. Pre-release samples in both years indicated that N. fresenii was not naturally present in A. gossypii populations in the San Joaquin Valley. Two release methods were compared: dried N. fresenii-infected cotton aphid “cadavers” and chamber inoculation of A. gossypii. Both methods were successful in introducing N. fresenii to cotton aphids in California; however, higher prevalence of fungal infection resulted with the cadaver treatments. N. fresenii persisted and spread in the aphid population until early October 1994 and late September 1995. The highest mean percentage infection in the cadaver treatment in 1994 reached a level (14%) considered imminent for epizootics (12–15%). The use of predator exclusion cages resulted in higher N. fresenii prevalences.     

Development of a Monoclonal Antibody for the Detection and Quantification of Predation on Slugs within the Arion hortensis agg. (Mollusca: Pulmonata)

The Arion hortensis agg. (Mollusca: Pulmonata) are major slug pests of agriculture and horticulture throughout much of the temperate World. A monoclonal antibody was created that could specifically identify and quantify the remains of these slugs within the carabid predator Pterostichus melanarius Illiger, a polyphagous species found in arable crops in Europe and North America. The antibody was shown to be specific for the two species of pest slug within this species aggregate, Arion distinctus Mabille and A. hortensis Férussac, and did not cross-react with any other invertebrates tested, including other slugs in the same genus. It proved to be highly sensitive in an enzyme-linked immunosorbent assay. The mean detection period for the remains of A. distinctus in predator foregut samples was 3.28 days at 16°C. However, A. distinctus remains could be identified in male carabids for 30% longer than in females, emphasizing the importance of separate analyses. The value of the antigen half-life as a measure of the detection period was questioned because analysis of covariance showed that the regression slopes for antigen decay were not significantly different between the two sexes, giving very similar half-lives (approx 18.5 h for females and 19 h for males). Calculated quantities of soluble slug proteins in predator foreguts declined more rapidly over time than concentrations, allowing separate assessment of the importance of these two variables on detection periods. It was concluded that a valuable new antibody had been created and characterized, which can be used for the analysis of predation in the field.     

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.     

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.     

Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies

The soybean aphid, Aphis glycines Matsumura, has become a principal arthropod pest of soybean in the U.S. since its first detection in 2000. This species threatens soybean production through direct feeding damage and virus transmission. A diverse guild of insect predators feeds on soybean aphid in Michigan including the exotic coccinellid Harmonia axyridis, the native gall midge Aphidoletes aphidimyza and the native lacewing Chrysoperla carnea. In addition to feeding on A. glycines some members of this guild may also engage in intraguild predation. These interactions may produce positive, negative, or neutral impacts on A. glycines biological control. We explored the impact of intraguild predation on soybean aphid population dynamics by comparing aphid populations in microcosms with either A. aphidimyza larvae or C. carnea larvae alone, with both a H. axyridis adult and either A. aphidimyza or C. carnea larvae, and without predators. When H. axyridis was present with larval A. aphidimyza or C. carnea, the lady beetle acted as an intraguild predator. However, intraguild feeding did not result in a release of aphid populations compared with microcosms containing only the intraguild and aphid prey. A similar result was found in field cages. Cages allowing large predators had reduced numbers of A. aphidimyza and C. carnea larvae but also significantly fewer aphids compared with predator exclusion cages. Thus, in both lab and field studies the direct impact of H. axyridis on A. glycines overcame its negative impact as an intraguild predator. Together, these studies indicate that while the exotic H. axyridis does act as an intraguild predator and may contribute to local declines in A. aphidimyza and C. carnea, it is also currently important in overall biological control of A. glycines.     

15N stable isotope labelling of slugs (Gastropoda: Pulmonata)

Stable isotope tracers are a promising tool for investigating the ecology of terrestrial slugs, including predator‐prey relationships, migration behaviour, nutrient turnover and dietary routing. The objective of the present feasibility study was to label two economically important slug groups, Deroceras reticulatum and keeled slugs (families Limacidae and Milacidae, respectively), with the stable isotope ¹⁵N under controlled laboratory conditions. Significant isotopic enrichment in slug tissue was detected after 4 days and persisted for at least 10 days after slugs had been fed on ¹⁵N enriched food for a period of 15 days. The time course of ¹⁵N uptake into slug tissues and its relation to food consumption were well described mathematically. Estimated mean ¹⁵N assimilation efficiencies from labelled maize mixed with unlabelled wheat bran were 30% and 38%, respectively, for the species groups studied. These findings suggest that slugs can be readily and efficiently labelled and that it is feasible to devise protocols for producing large numbers of isotopically labelled slugs for use in ecological studies. A simple method is described for the collection and analysis of cutaneous mucus from individual slugs which can be used to test uniformity of isotopic labelling.     

Effects of feeding frequency and sugar concentration on behavior and longevity of the adult aphid parasitoid: Aphidius ervi (Haliday) (Hymenoptera: Braconidae)

The effectiveness of the predatory mite, Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseidae), as a suppressive agent of the twospotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), was evaluated on greenhouse ivy geraniums at predator:prey release ratios of 1:60, 1:20, and 1:4. Releases at each predator:prey ratio were made at moderate and high T. urticae densities to determine if initial pest population size influenced the suppressive ability of the predator. At ratios of 1:4 and 1:20, P. persimilis significantly reduced T. urticae populations 1 week after release and kept them at low levels thereafter. Plant damage also was significantly reduced at these densities. After 4 weeks, the P. persimilis that were released at a ratio of 1:4 consistently reduced T. urticae populations from densities as high as 30 T. urticae per leaf to fewer than 0.6 per leaf. We found no interaction between release ratio and T. urticae density, indicating that predator effectiveness remains constant, at least within the range of T. urticae densities used. Our work demonstrates the potential of P. persimilis to provide effective control of T. urticae on a greenhouse-grown floricultural crop at a moderately low predator:prey ratio (1:20) and over a range of initial pest densities. However, we recommend that P. persimilis be released at a ratio of 1:4 for greatest reliability and successful control of T. urticae on ivy geraniums.     

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.     

Predation by Podisus maculiventris (Hemiptera: Pentatomidae) on Plutella xylostella (Lepidoptera: Plutellidae) larvae parasitized by Cotesia plutellae (Hymenoptera: Braconidae) and its impact on cabbage

Biological control offers potentially effective suppression of the diamondback moth (DBM), Plutella xylostella, a serious pest of Brassica crops. Little is known of whether multiple natural enemies have additive, antagonistic, or synergistic effects on DBM populations. No-choice and choice tests were conducted to assess predation by Podisus maculiventris on DBM larvae parasitized by Cotesia plutellae and unparasitized larvae. In no-choice tests, P. maculiventris preyed on greater numbers of parasitized than unparasitized larvae and greater numbers of young larvae than old larvae. In choice tests with early third instar DBM, there was no difference in predation between parasitized or unparasitized larvae. However, in choice tests with older prey, P. maculiventris preyed on more parasitized than unparasitized larvae. Two field studies were conducted to test if this predator and parasitoid have additive, antagonistic or synergistic effects on DBM populations and plant damage in cabbage (Brassica oleracea var. capitata). In 2002, DBM populations were significantly lower in the presence of C. plutellae but not in the presence of P. maculiventris. There was not a significant interaction between the natural enemies. Plant damage was reduced only with C. plutellae. In 2003, DBM populations were significantly lower in the presence of C. plutellae and P. maculiventris, although the combination of natural enemies did not lead to a non-additive interaction. Plant damage was unaffected by the presence of either natural enemy. Because of its greater predation on parasitized larvae, P. maculiventris could be an intraguild predator of C. plutellae. Yet, their overall combined effect in the field was additive rather than antagonistic.     

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

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

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.     

Larval feeding behaviour of Tetanocera elata (Diptera: Sciomyzidae): potential biocontrol agent of pestiferous slugs

Examining predatory behaviour is useful for determining the potential of novel biocontrol agents. We investigated the predatory behaviour of Tetanocera elata (Fabricius) larvae on the pestiferous slug Deroceras reticulatum (Müller). Results indicate three prey-finding strategies, including the predator reaching its prey without previous contact with it or its mucus trail.     

Decay rates for slug antigens within the carabid predatorPterostichus melanarius monitored with a monoclonal antibody

The rate at which prey antigens decay within a predator during digestion must be calibrated, for a given assay system, in order to define the period within which predation must have occurred. Monoclonal antibodies have great advantages in terms of target specificity, but have often in the past demonstrated impractically abbreviated antigen detection periods. However, the DrW-2D11 monoclonal antibody, which detects all three genera of pest slugs (Mollusca: Pulmonata) in Britain, could clearly identify predation byPterostichus melanarius Illiger (Coleoptera: Carabidae) after 2.5 days at 16°C, a longer interval than has been recorded for any other monoclonal antibody used in predation studies. The half-life, detection period and decay rate were calibrated with and without subsequent feeding on alternative prey. Unrestricted feeding on earthworm, following consumption of the slugDeroceras reticulatum (Müller), significantly reduced the decay rate of slug antigens. These results appear to contradict the assumptions, based on previous studies, that indicate reduced digestion rates in response to starvation. Possible reasons for this failure to comply with the predictions of optimal foraging theories 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.     

Neoseiulus Californicus (Acari: Phytoseiidae) as a Potential Control Agent of Tetranychus Urticae (Acari: Tetranychidae): Effect of Pest/Predator Ratio on Pest Abundance on Strawberry

Neoseiulus californicus (McGregor) is a promising agent for successful Tetranychus urticae Koch control through conservation techniques, in strawberry crops in La Plata (Buenos Aires, Argentina). In prey–predator interaction, initial relative densities have an important effect on system dynamics. The economic threshold level (ETL) used for this pest in the present study was 50 active mites per leaflet. In our laboratory experiments, initial T. urticae to N. californicus ratio had a significant effect on the population abundance of T. urticae at a 7-day period. When pest/predator ratio was 5/1 (at initial pest densities from 5 to 15 females/leaflet) the final number of active T. urticae/leaflet was significantly lower than the ETL, while at 20 females/leaflet this number did not differ from the ETL. At 7.5/1 ratio, the final number of active T. urticae/leaflet, at initial pest densities from 5 to 15 females/leaflet, reached the ETL without surpassing it. At 10/1 and 15/1 ratios, pest densities exceeded the ETL only at 15 initial T. urticae/leaflet. Most greenhouse and field observations were consistent with the predictions of a graphical model based on experimental results. This predator was very effective in limiting pest densities at a 7-day period and within the range of pest–predator ratios and absolute densities used in this study. Conservation of N. californicus promoting favorable pest/predator ratios may result in early control of T. urticae.     

Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii

Colonization of tomato greenhouses by native predatory mirid bugs at the end of the spring cycle is common in the western Mediterranean area when no broad-spectrum insecticides are applied. Due to their polyphagy, these predators interact with pest populations and also with other natural enemies present in the crop. In this work we evaluate the abundance and timing of greenhouse colonization by these predators and their interaction with the greenhouse whitefly Trialeurodes vaporariorum, a key crop pest, and its introduced parasitoid Encarsia formosa. Although quite unpredictable, natural colonization of greenhouses by Macrolophus caliginosus and Dicyphus tamaninii, the two predominant species in our location, usually leads to the establishment of predator populations in the crop that subsequently prey on greenhouse whitefly. No preference for parasitized pupae was observed in greenhouse samples, while laboratory experiments revealed a marked tendency to avoid parasitoid pupae. In our area, IPM programs for greenhouse tomatoes and other vegetables should take advantage of the presence of this predator complex by allowing the immigration and establishment of its populations without disturbing them with highly toxic and non-selective insecticides.     

Identification of priority areas in South America for exploration of natural enemies for classical biological control of Tetranychus evansi (Acari: Tetranychidae) in Africa

The red spider mite Tetranychus evansi Baker and Pritchard is a pest of tomato in East and Southern Africa. It is probably native to South America. Three models were established to identify priority areas for the search of natural enemies in South America for classical biological control of this pest in Africa. The models were based on the concept of “fundamental ecological niche”, predicting regions in South America that have similar environmental conditions to areas where the mite is a problem in Africa, using Desktop-GARP (Genetic Algorithm for Rule-set Production). Based on the model established with data sets from Kenya and Zimbabwe, it was determined that priority areas include areas in Brazil, Argentina, Paraguay and Uruguay, as well as some restricted areas in other South American countries.     

Interactions of two natural enemies of Tetranychus evansi, the fungal pathogen Neozygites floridana (Zygomycetes: Entomophthorales) and the predatory mite, Phytoseiulus longipes (Acari: Phytoseiidae)

Tetranychus evansi is an exotic pest of Solanaceous crops in Africa discovered in Zimbabwe in 1979. Two natural enemies, the predatory mite Phytoseiulus longipes and the fungal pathogen Neozygites floridana are important causes of mortality in T. evansi populations in Brazil. The first part of this study assessed the effects of N. floridana on predation and oviposition of P. longipes fed on N. floridana infected T. evansi and T. urticae. No N. floridana hyphal bodies were found in P. longipes after this feeding, demonstrating that N. floridana is not pathogenic to P. longipes and does not affect its oviposition. The second part of the study investigated the time spent on searching for and consuming of eggs on leaf discs with and without N. floridana capilliconidia. Both the searching and the feeding time on the first egg were similar on leaf discs with and without capilliconidia. When P. longipes was offered the choice of feeding on eggs on leaf discs with or without capilliconidia, the numbers of eggs consumed were not different. The only N. floridana effect observed on P. longipes was reduced egg predation. In addition, increased time spent grooming on leaf discs with capilliconidia was observed. P. longipes was efficient in removing most capilliconidia attached to the body through self-grooming behavior. This suggests that although the predator did not avoid areas with capilliconidia, it detected and removed most capilliconidia attached to the body. Increased grooming may account for the lower egg predation rates.