A Species-specific Monoclonal Antibody System for Detecting the Remains of Field Slugs, Deroceras reticulatum (Muller) (Mollusca: Pulmonata), in Carabid Beetles (Coleoptera: Carabidae)

The field slug, Deroceras reticulatum (Muller), is probably the most damaging and widespread species of slug, causing severe economic losses in a broad range of crops in temperate zones throughout the world. Investigations into the role of predation in the population dynamics of this species required a biochemical system which was capable of identifying the remains of this slug in the crop contents of predators, and distinguishing them from those of other molluscs. A monoclonal antibody was developed (IgM isotype). This was capable of separating, in an enzyme-linked immunosorbent assay, D. reticulatum from the related D. caruanae (Pollonera) and all molluscs and other invertebrates tested, with the unexpected exceptions of New Zealand flatworms, Artioposthia triangulata (Deny) and the millipede Polymicrodon polydesmoides (Leach). Characterization of the antibody and assay demonstrated that the system could clearly detect as little as 11.6 ng of D. reticulatum protein in 200 mu l of buffer. Slug remains could be identified as such in the crops of the carabid predator Pterostichus melanarius Illiger for 38.1 h, while the antibody-antigen reaction declined to half of that measured immediately following consumption, after 12.9 h. A practical and highly sensitive system was therefore developed, using the first species-specific monoclonal antibody available for the investigation of predation on slugs.     

Do earthworms help to sustain the slug predator Pterostichus melanarius (Coleoptera: Carabidae) within crops? Investigations using monoclonal antibodies

Earthworms provide a major potential source of alternative food for polyphagous predators, such as carabid beetles, that are natural enemies of slugs, aphids and other agricultural pests. Non-pest prey may foster larger numbers of natural enemies, which then help to control pests, or alternatively may help to divert the predators away from pest control. An earthworm-specific monoclonal antibody was developed to study carabid-earthworm interactions in the field and assess the role of earthworms as alternative prey. The antibody could identify as little at 7 ng of earthworm protein in an ELISA, and could detect earthworm remains in the foregut of the carabid beetle Pterostichus melanarius for 64 h after consumption. Thirty-six per cent of field-collected beetles contained earthworm remains. Quantities of earthworm proteins in the beetle foreguts were negatively related to total foregut biomass, suggesting that earthworm consumption increased as total prey availability declined. There was also a negative relationship between foregut biomass and beetle numbers, but both quantities and concentrations of earthworm proteins in beetle foreguts were positively related to beetle numbers. This suggests that as beetle activity-density increased, total prey availability declined, or, as prey availability declined, beetles spent more time searching. In these circumstances, beetles fed to a greater extent on earthworms, an acceptable but nonpreferred food item. Earthworms may, therefore, provide an ideal alternative prey for P. melanarius, helping to sustain it when pest numbers are low but allowing it to perform a 'lying-in-wait' strategy, ready to switch back to feeding on pests when they become available.     

Development of specific ITS markers for plant DNA identification within herbivorous insects

DNA-based techniques have proved to be very useful methods to study trophic relationships between pests and their natural enemies. However, most predators are best defined as omnivores, and the identification of plant-specific DNA should also allow the identification of the plant species the predators have been feeding on. In this study, a PCR approach based on the development of specific primers was developed as a self-marking technique to detect plant DNA within the gut of one heteropteran omnivorous predator (Macrolophus pygmaeus) and two lepidopteran pest species (Helicoverpa armigera and Tuta absoluta). Specific tomato primers were designed from the ITS 1-2 region, which allowed the amplification of a tomato DNA fragment of 332?bp within the three insect species tested in all cases (100% of detection at t=0) and did not detect DNA of other plants nor of the starved insects. Plant DNA half-lives at 25°C ranged from 5.8?h, to 27.7?h and 28.7?h within M. pygmaeus, H. armigera and T. absoluta, respectively. Tomato DNA detection within field-collected M. pygmaeus suggests dietary mixing in this omnivorous predator and showed a higher detection of tomato DNA in females and nymphs than males. This study provides a useful tool to detect and to identify plant food sources of arthropods and to evaluate crop colonization from surrounding vegetation in conservation biological control programs.     

DOES TANDONIA BUDAPESTENIS (MOLLUSCA: PULMONATA) CONTAIN TOXINS? EVIDENCE FROM FEEDING TRIALS WITH THE SLUG PREDATOR PTEROSTICHUS MELANARIUS (COLEOPTERA: CARABIDAE)

Slugs are known to be killed and consumed by a range of invertebrateand vertebrate predators in the field. Carabid beetles (Coleoptera:Carabidae) in particular are major natural enemies of slugs,and have been shown to be capable of controlling certain speciesin a crop environment. This paper reports experiments to investigatethe effects, on the carabid Pterostichus melanarius, of feedingon the milacid slug Tandonia budapestensis. The slugs provedto be toxic, 50% of the beetles dying within two days. Mortalityof beetles fed on two other species of slug, Deroceras reticulatumand Arion distinctus, was not significantly different from thatfor beetles fed upon a control prey (Calliphora vomitoria).These results represent the only known case of a European slugproving to be toxic to potential predators, and is one of avery small number of reported instances of possible toxicityamongst terrestrial gastropods. The possibility that the orangeline down the dorsal keel of T. budapestensis may act as warningcoloration to birds is discussed. (Received 4 December 1996; accepted 5 March 1997)     

Search for effective natural enemies of <Emphasis Type="Italic">Tetranychus evansi</Emphasis> (Acari: Tetranychidae) in northwest Argentina

The mite Tetranychus evansi Baker & Pritchard (Tetranychidae) probably originated in South America. Because of its importance as a tomato pest in Africa, an extensive project has been conducted to detect potentially effective natural enemies in South America for the classical biological control of the pest in Africa. A search for the natural enemies of T. evansi was conducted in the Province of Tucumán, northwestern Argentina, in December 2004, and this report describes the results. One hundred predatory mites of the family Phytoseiidae referring to 11 species were collected on 11 examined species of solanaceous plants. The most abundant phytoseiid species collected were Neoseiulus californicus (McGregor) and Euseius concordis (Chant). Adults and immatures of those species, as well as of Neoseiulus idaeus Denmark & Muma, Phytoseiulus fragariae Denmark & Schicha and Proprioseiopsis cannaensis (Muma) were found in association with T. evansi, suggesting that they were developing on the pest. However, because of the possible biological differences between populations of a given species, biological studies evaluating T. evansi as a prey for those predators seem desirable.     

Tetanocera elata (Diptera: Sciomyzidae) Larvae Feed on Protected Slug Species Geomalacus maculosus (Gastropoda: Arionidae): First Record of Predation

The Family Sciomyzidae (Diptera) is one of the best studied groups of malacophagous insects containing some of the most important enemies of slugs. Larvae of the fly Tetanocera elata are known obligate feeders on slugs both as parasitoids and predators. We tested whether predatory larvae of T. elata can feed on the protected slug species Geomalacus maculosus, for which there appear to be no published records of natural enemies. Using an infra-red video camera, we recorded the behaviour of third instar T. elata in the presence of: 1) a single specimen of G. maculosus and 2) one specimen each of G. maculosus and Deroceras reticulatum, a known slug prey of T. elata. We describe the behaviour of the larvae where they killed and consumed G. maculosus and D. reticulatum in experiments 1 and 2 respectively. Since T. elata has been suggested as a potential biocontrol agent of pestiferous slugs, the possibility of predation on the protected species G. maculosus is discussed from this perspective.     

Species distribution models for natural enemies of monarch butterfly (<Emphasis Type="Italic">Danaus plexippus</Emphasis>) larvae and pupae: distribution patterns and implications for conservation

Prey populations can be strongly influenced by predators and parasitoids, and migratory prey whose distributions vary geographically throughout their breeding seasons encounter different combinations of predators and parasitoids throughout their range. North American monarch butterflies (Danaus plexippus) are susceptible to a wide variety of natural enemies, but the distribution of these natural enemies has not been quantified. We developed ecological niche models using environmental data to identify areas with suitable abiotic conditions for eight known natural enemies of monarchs, including six predators: Arilus cristatus, Harmonia axyridis, Monomorium minimum, Podisus maculiventris, Polistes spp., and Solenopsis geminata; and two parasitoids: Lespesia archippivora and Pteromalus cassotis. We combined correlated suitable areas for individual predators and parasitoids to identify regions with the most predator and parasitoid species potential. The Gulf Coast, West Coast, Florida, and parts of the eastern United States are predicted to have the most natural enemy species. We suggest that future research should assess monarch mortality rates in these areas, and that monarch conservation strategies consider pressure from natural enemies.     

Hibernation of predatory arthropods in semi-natural habitats

Non-crop habitats provide important resources for natural enemies. Many natural enemies hibernate in non-crop habitats, from which they may colonise arable fields in the spring. Spring colonisation ensures annual repopulation of the crop with natural enemies, allowing them to keep pace with the development of pest populations. The availability of non-crop habitats can, therefore, be crucial to successful conservation biological control. We quantified the density of overwintering natural enemies near organic Brussels sprout crops in five different non-crop habitats (short grassy field margin, herbaceous field margin, herbaceous field margin under a tree line, ditch and forest). Soil and litter samples of non-crop habitats were taken at two sites. One site was located in an open agricultural landscape, the other in a landscape dominated by mixed forest. Insects belonging to Staphylinidae, Araneae, Carabidae, Coccinellidae and Dermaptera were the most abundant. Mean densities of predatory arthropods were higher in the open agricultural landscape (290 predators m⁻²) than in the forested landscape (137 predators m⁻²). Herbaceous habitat types supported the highest densities of overwintering predators (up to 400 predators m⁻²), whereas densities in the forest were lowest (10 predators m⁻²). These results indicate that herbaceous non-crop habitats are important refugia for predators and may play a vital role in conservation biological control. Handling Editor: Arne Janssen.     

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.     

Evolution and losses of spines in slug caterpillars (Lepidoptera: Limacodidae)

Larvae of the cosmopolitan family Limacodidae, commonly known as “slug” caterpillars, are well known because of the widespread occurrence of spines with urticating properties, a morpho‐chemical adaptive trait that has been demonstrated to protect the larvae from natural enemies. However, while most species are armed with rows of spines (“nettle” caterpillars), slug caterpillars are morphologically diverse with some species lacking spines and thus are nonstinging. It has been demonstrated that the evolution of spines in slug caterpillars may have a single origin and that this trait is possibly derived from nonstinging slug caterpillars, but these conclusions were based on limited sampling of mainly New World taxa; thus, the evolution of spines and other traits within the family remains unresolved. Here, we analyze morphological variation in slug caterpillars within an evolutionary framework to determine character evolution of spines with samples from Asia, Australia, North America, and South America. The phylogeny of the Limacodidae was reconstructed based on a multigene dataset comprising five molecular markers (5.6 Kbp: COI, 28S, 18S, EF‐1α, and wingless) representing 45 species from 40 genera and eight outgroups. Based on this phylogeny, we infer that limacodids evolved from a common ancestor in which the larval type possessed spines, and then slug caterpillars without spines evolved independently multiple times in different continents. While larvae with spines are well adapted to avoiding generalist predators, our results imply that larvae without spines may be suited to different ecological niches. Systematic relationships of our dataset indicate six major lineages, several of which have not previously been identified.     

Natural enemy responses and pest control: Importance of local vegetation

Natural invertebrate enemies on farmland may respond to local vegetation adjacent to the farmland. This can encourage individual landholders to maintain vegetation even when there are costs in terms of a reduction in crop area as well as maintenance of the vegetation. Here we investigated abundance of natural enemies in 61 vineyards from south eastern Australia, with either adjacent woody vegetation consisting of remnant native forests or wooded margins planted after establishment of the crop, or lacking in adjacent vegetation. Invertebrates were sampled five times at monthly intervals using canopy sticky traps. There was an increase in abundance of different groups of natural enemies when woody vegetation was present although these increases depended on size. Small natural enemies tended to be influenced by local features, whereas larger potentially more mobile groups were not affected. Predation of eggs of a vineyard insect pest, Epiphyas postvittana, was relatively higher in vineyards with either adjacent remnant forest or planted woody vegetation. Various types of local vegetation may therefore encourage a range of predators and parasitoids, increasing predation and control of a common vineyard pest.     

Edges in Agricultural Landscapes: Species Interactions and Movement of Natural Enemies

Agricultural landscapes can be characterized as a mosaic of habitat patches interspersed with hostile matrix, or as a gradient of patches ranging from suitable to unsuitable for different species. Arthropods moving through these landscapes encounter a range of edges, with different permeability. Patches of native vegetation in these landscapes may support natural enemies of crop pests by providing alternate hosts for parasitic wasps and/or acting as a source for predatory insects. We test this by quantifying species interactions and measuring movement across different edge-types. A high diversity of parasitoid species used hosts in the native vegetation patches, however we recorded few instances of the same parasitoid species using hosts in both the native vegetation and the crop (canola). However, we did find overall greater densities of parasitoids moving from native vegetation into the crop. Of the parasitoid groups examined, parasitoids of aphids (Braconidae: Aphidiinae) frequently moved from native vegetation into canola. In contrast, parasitoids of caterpillars (Braconidae: Microgastrinae) moved commonly from cereal fields into canola. Late season samples showed both aphids and parasitoids moving frequently out of native vegetation, in contrast predators moved less commonly from native vegetation (across the whole season). The season-long net advantage or disadvantage of native vegetation for pest control services is therefore difficult to evaluate. It appears that the different edge-types alter movement patterns of natural enemies more so than herbivorous pest species, and this may impact pest control services.     

农田非作物生境调控与害虫综合治理

就害虫综合治理的研究而言,农田生态系统可以区分出作物生境和邻近作物的非作物生境。昆虫从作物生境迁移到非作物生境,与作物生境缺乏食物或受人类栽培活动干扰而引起的自然迁移、转换寄主和寻求庇护场所有关。许多研究表明,与特定作物田块相联系的植被类型和结构可影响害虫及其天敌迁居的种类、数量和时间。因此,我们可以通过改变大田周围非作物生境的植被组成及特征来调控农业生态系统中害虫与天敌的相互关系,提高天敌对害虫的控制效能。由于景观的空间格局对节肢动物的生物学特性有直接或间接的影响,所以,以景观为单元要比以同类作物的田块为单元更加适于害虫综合治理的研究和实施。在现代农业景观区域内重新引入和相嵌一些非栽培植物或廊道,可为众多有益节肢动物的繁殖、取食和避害提供多种类型的非作物栖境。     

Preface

Data on the toxicity and selectivity of synthetic pyrethroids (SPs) to arthropod natural enemies and their host or prey are reviewed with emphasis on cotton, apple, alfalfa, cereal and vegetable inhabiting species. Generally, SPs are variably toxic and selective (in relation to their hosts or prey) to species within most families of natural enemies. Exceptions are low to moderate toxicity and favorable selectivity to most hemipteran predators, and high toxicity and unfavorable selectivity to virtually all phytoseiid mites in comparison to their prey. In North America, SPs are more favorably selective to cotton natural enemies over their prey or host than to apple inhabiting species. These differences may be due to intrinsic levels of susceptibility (preselection levels) between the types of natural enemies exploited on both crops in IPM programs (i.e. hemipteran species on cotton versus phytoseiid mites on apple) and/or to tolerances or resistances differences due to previous patterns of chemical use on these crops. Possible means of increasing selective use of SPs in future IPM systems based on ecological and physiological selectivity including the development of SP-resistant predators are discussed.     

Records of Natural Enemies of Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae) Biotype B in Brazil

Collections of natural enemies of Bemisia tabaci biotype B (Genn.) (Hemiptera: Aleyrodidae) were made in Lavras, state of Minas Gerais, Brazil. In the greenhouse, 6,495 predators and 16,628 parasitoids belonging to three families were collected. In the field, 267 predators and 344 parasitoids belonging to five families were found. For the first time in Brazil, five species of predators associated with this whitefly were reported. Because of the diversity of natural enemies of B. tabaci biotype B recorded, this study points out the importance of these data for studies on integrated pest management.     

The role of natural enemy guilds in Aphis glycines suppression

Generalist natural enemy guilds are increasingly recognized as important sources of mortality for invasive agricultural pests. However, the net contribution of different species to pest suppression is conditioned by their biology and interspecific interactions. The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is widely attacked by generalist predators, but the relative impacts of different natural enemy guilds remains poorly understood. Moreover, low levels of A. glycines parasitism suggest that resident parasitoids may be limited through intraguild predation. During 2004 and 2005, we conducted field experiments to test the impact of different guilds of natural enemies on A. glycines. We contrasted aphid abundance on field cages with ambient levels of small predators (primarily Orius insidiosus) and parasitoids (primarily Braconidae), sham cages and open controls exposed to large predators (primarily coccinellids), and cages excluding all natural enemies. We observed strong aphid suppression (86- to 36-fold reduction) in treatments exposed to coccinellids, but only minor reduction due to small predators and parasitoids, with aphids reaching rapidly economic injury levels when coccinellids were excluded. Three species of resident parasitoids were found attacking A. glycines at very low levels (<1% parasitism), with no evidence that intraguild predation by coccinellids attenuated parasitoid impacts. At the plant level, coccinellid impacts resulted in a trophic cascade that restored soybean biomass and yield, whereas small natural enemies provided only minor protection against yield loss. Our results indicate that within the assemblage of A. glycines natural enemies in Michigan, coccinellids are critical to maintain aphids below economic injury levels.     

农田景观格局对害虫天敌生态控害功能的调控作用

如何提升农田景观的生态服务功能是当前景观生态学和害虫防治学的前沿研究热点.基于区域农田景观格局可显著调节植物-植食性昆虫-天敌之间相互关系的理论基础,本文系统概括总结了农田景观格局及其变化对农田重要天敌多样性与生态控害功能的影响.从不同天敌类群的角度,分析了农田景观格局对捕食性天敌、寄生性天敌、有益微生物及其生态控害功能的调控作用.同时,对优化农田景观作物布局、采取合理的植被生境管理策略进行了展望.本文可为应用植被生境管理提升农田景观中天敌的生态系统服务功能提供参考,进一步促进区域生态农业响应"化学农药减量施用"的战略目标提供理论支撑.     

Avoidance of natural enemies by adult whiteflies, Bemisia argentifolii, and effects on host plant choice

In this study we asked whether, in the context of a trap crop system, differential predation risks among plants influence host choice patterns of adult whiteflies, Bemisia argentifolii. We investigated whether adult whiteflies avoid natural enemies inhabiting poinsettia (a cash crop) and whether this behavior can be used to increase the movement of whiteflies to cucumber (a trap crop). The potential of cucumber as a trap crop was first evaluated and we found that significantly more whiteflies were attracted to cucumber when the whiteflies were released between the two plants. However, the accumulation of whiteflies on cucumber substantially diminished if the insects had first settled on poinsettia. Under such circumstances, we investigated whether movement of adult whiteflies to cucumber could be increased by creating conditions that would cause the whiteflies that had settled on poinsettia to leave the plant. A mechanical disturbance, consisting of shaking the plant, was first used to test this hypothesis. The shaking caused more whiteflies to leave poinsettia and move onto the trap crop, compared to undisturbed whiteflies. We then asked whether the presence of natural enemies on the cash crop could induce whiteflies to leave the cash crop and move onto the trap crop. Three natural enemies were tested: two predators, Amblyseius swirskii and Delphastus catalinae, and a parasitoid Encarsia formosa. The presence of D. catalinae on poinsettia induced significantly more whiteflies to disperse to cucumber compared to poinsettia with no natural enemies, whereas A. swirskii and E. formosa did not result in a significant increase. Predator avoidance behavior by adult whiteflies should be investigated further in the context of trap cropping and other crop-habitat alterations designed to help manage whitefly abundance.     

The impact of transgenic plants on natural enemies: a critical review of laboratory studies

We reviewed laboratory tests which studied the impact of genetically modified plants on arthropod natural enemies. A total of 18 species of predators and 14 species of parasitoids have been tested, most in only a few experiments. Certain groups (braconid wasps) or species (the green lacewing, Chrysoperla carnea) have attracted much effort, while representatives of others, including whole orders (e.g., Diptera), have never had a species tested. We conclude that laboratory tests are not the ‘worst case’ scenarios intended by the experimental designs, and are not often ecologically realistic: they typically provided ad libitum feeding, no prey choice, single prey type, no combination of stress factors and usually uniform temperatures. None of these are representative of field conditions, yet most could be easily mimicked in more complex laboratory tests. In most cases (94.6%), the studies were unable to indicate the level of power required to detect any impact. Small sample size and large variability are factors that mask all but very large differences in potential effects. For predators, 126 parameters were quantified, most commonly including survival/mortality (37 cases), development time (22), and body mass/size (20). For parasitoids, 128 parameters were quantified, the majority involving lectins or proteinase inhibitors. Most frequent measurements were: fecundity (23 experiments), adult longevity, extent of parasitism (17 each), body size, mortality, and larval development time. An aggregative scoring (summarising all quantified parameters) indicated that the laboratory tests quantified a remarkable number of cases (30% for predators, 39.8% for parasitoids), where the impacts of the genetically modified plant were significantly negative. These involve various parameters, organisms, test methods, and significance levels, but collectively they indicate that the use of genetically modified crops may result in negative effects on the natural enemies of crop pests.     

Effects of crop species richness on pest-natural enemy systems based on an experimental model system using a microlandscape

The relationship between crop richness and predator-prey interactions as they relate to pest-natural enemy systems is a very important topic in ecology and greatly affects biological control services. The effects of crop arrangement on predator-prey interactions have received much attention as the basis for pest population management. To explore the internal mechanisms and factors driving the relationship between crop richness and pest population management, we designed an experimental model system of a microlandscape that included 50 plots and five treatments. Each treatment had 10 repetitions in each year from 2007 to 2010. The results showed that the biomass of pests and their natural enemies increased with increasing crop biomass and decreased with decreasing crop biomass; however, the effects of plant biomass on the pest and natural enemy biomass were not significant. The relationship between adjacent trophic levels was significant (such as pests and their natural enemies or crops and pests), whereas non-adjacent trophic levels (crops and natural enemies) did not significantly interact with each other. The ratio of natural enemy/pest biomass was the highest in the areas of four crop species that had the best biological control service. Having either low or high crop species richness did not enhance the pest population management service and lead to loss of biological control. Although the resource concentration hypothesis was not well supported by our results, high crop species richness could suppress the pest population, indicating that crop species richness could enhance biological control services. These results could be applied in habitat management aimed at biological control, provide the theoretical basis for agricultural landscape design, and also suggest new methods for integrated pest management.