Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers

Collembola comprise a major source of alternative prey to linyphiid spiders in arable fields, helping to sustain and retain these predators as aphid control agents within the crop. Polymerase chain reaction primers were developed for the amplification, from spider gut samples, of DNA from three of the most abundant species of Collembola in wheat crops in Europe, namely Isotoma anglicana, Lepidocyrtus cyaneus and Entomobrya multifasciata. The primers amplified fragments of the mitochondrial cytochrome oxidase subunit I (COI) gene and were designed following alignment of comparable sequences for a range of predator and prey species. Each of the primer pairs proved to be species-specific to a Collembola species, amplifying DNA fragments from 211 to 276 base pairs in length. Following consumption of a single collembolan, prey DNA was detectable in 100% of spiders after 24 h of digestion. We report the first use of DNA-based techniques to detect predation by arthropods on natural populations of prey in the field. All three species of Collembola were consumed by the spiders. By comparing the ratios of the Collembola species in the field with the numbers of spiders that gave positive results for each of those species, it was possible to demonstrate that the spiders were exercising prey choice. Overall, a single target species of Collembola was eaten by 48% of spiders while a further 16% of spiders contained DNA from two different species of Collembola. Preference was particularly evident for I. anglicana, the species most frequently found in spider guts yet the least numerous of the three target species in the field.     

Prey DNA detection success following digestion by intraguild predators: influence of prey and predator species

Intraguild predation (IGP) has been increasingly recognized as an important interaction in ecological systems over the past two decades, and remarkable insights have been gained into its nature and prevalence. We have developed a technique using molecular gut-content analysis to compare the rate of IGP between closely related species of coccinellid beetles (lady beetles or ladybirds), which had been previously known to prey upon one another. We first developed PCR primers for each of four lady beetle species: Harmonia axyridis, Coccinella septempunctata, Coleomegilla maculata and Propylea quatuordecimpunctata. We next determined the prey DNA detection success over time (DS(50) ) for each combination of interacting species following a meal. We found that DS(50) values varied greatly between predator-prey combinations, ranging from 5.2 to 19.3 h. As a result, general patterns of detection times based upon predator or prey species alone are not discernable. We used the DS(50) values to correct field data to demonstrate the importance of compensation for detection times that are specific to particular predator-prey combinations.     

Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach

The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is a pest of soybeans in Asia, and in recent years has caused extensive damage to soybeans in North America. Within these agroecosystems, generalist predators form an important component of the assemblage of natural enemies, and can exert significant pressure on prey populations. These food webs are complex and molecular gut-content analyses offer nondisruptive approaches for examining trophic linkages in the field. We describe the development of a molecular detection system to examine the feeding behaviour of Orius insidiosus (Hemiptera: Anthocoridae) upon soybean aphids, an alternative prey item, Neohydatothrips variabilis (Thysanoptera: Thripidae), and an intraguild prey species, Harmonia axyridis (Coleoptera: Coccinellidae). Specific primer pairs were designed to target prey and were used to examine key trophic connections within this soybean food web. In total, 32% of O. insidiosus were found to have preyed upon A. glycines, but disproportionately high consumption occurred early in the season, when aphid densities were low. The intensity of early season predation indicates that O. insidiosus are important biological control agents of A. glycines, although data suggest that N. variabilis constitute a significant proportion of the diet of these generalist predators. No Orius were found to contain DNA of H. axyridis, suggesting intraguild predation upon these important late-season predators during 2005 was low. In their entirety, these results implicate O. insidiosus as a valuable natural enemy of A. glycines in this soybean agroecosystem.     

Pikeperch Sander lucioperca trapped between niches: foraging performance and prey selection in a piscivore on a planktivore diet

The foraging behaviour of planktivorous pikeperch Sander lucioperca during their first growing season was analysed. Field data showed that S. lucioperca feed on extremely rare prey at the end of the summer, suggesting the presence of a bottleneck. In experiments, foraging ability of planktivorous S. lucioperca was determined when fish were feeding on different prey types (Daphnia magna or Chaoborus spp.) and sizes (D. magna of lengths 1 or 2·5 mm) when they occurred alone. From these results, the minimum density requirement of each prey type was analysed. The energy gain for three different foraging strategies was estimated; a specialized diet based on either large D. magna or Chaoborus spp. or a generalist diet combining both prey types. Prey value estimates showed that Chaoborus spp. should be the preferred prey, assuming an energy maximizing principle. In prey choice experiments, S. lucioperca largely followed this principle, including D. magna in the diet only when the density of the Chaoborus spp. was below a threshold value. Splitting the foraging bout into different sequences, however, resulted in a somewhat different pattern. During an initial phase, S. lucioperca captured both prey as encountered and then switched to Chaoborus spp. if prey density was above the threshold level. The prey selection observed was mainly explained by sampling behaviour and incomplete information about environmental quality, whereas satiation only had marginal effects. It was concluded that the observed diet based on rare prey items was in accordance with an optimal foraging strategy and may generate positive growth in the absence of prey fish in suitable sizes.     

Methods to identify the prey of invertebrate predators in terrestrial field studies

Predation is an interaction during which an organism kills and feeds on another organism. Past and current interest in studying predation in terrestrial habitats has yielded a number of methods to assess invertebrate predation events in terrestrial ecosystems. We provide a decision tree to select appropriate methods for individual studies. For each method, we then present a short introduction, key examples for applications, advantages and disadvantages, and an outlook to future refinements. Video and, to a lesser extent, live observations are recommended in studies that address behavioral aspects of predator–prey interactions or focus on per capita predation rates. Cage studies are only appropriate for small predator species, but often suffer from a bias via cage effects. The use of prey baits or analyses of prey remains are cheaper than other methods and have the potential to provide per capita predation estimates. These advantages often come at the cost of low taxonomic specificity. Molecular methods provide reliable estimates at a fine level of taxonomic resolution and are free of observer bias for predator species of any size. However, the current PCR‐based methods lack the ability to estimate predation rates for individual predators and are more expensive than other methods. Molecular and stable isotope analyses are best suited to address systems that include a range of predator and prey species. Our review of methods strongly suggests that while in many cases individual methods are sufficient to study specific questions, combinations of methods hold a high potential to provide more holistic insights into predation events. This review presents an overview of methods to researchers that are new to the field or to particular aspects of predation ecology and provides recommendations toward the subset of suitable methods to identify the prey of invertebrate predators in terrestrial field research.     

Selectivity underlies the dissociation between seasonal prey availability and prey consumption in a generalist predator

Generalist predators are capable of selective foraging, but are predicted to feed in close proportion to prey availability to maximize energetic intake especially when overall prey availability is low. By extension, they are also expected to feed in a more frequency‐dependent manner during winter compared to the more favourable foraging conditions during spring, summer and fall seasons. For 18 months, we observed the foraging patterns of forest‐dwelling wolf spiders from the genus Schizocosa (Araneae: Lycosidae) using PCR‐based gut‐content analysis and simultaneously monitored the activity densities of two common prey: springtails (Collembola) and flies (Diptera). Rates of prey detection within spider guts relative to rates of prey collected in traps were estimated using Roualdes’ c_st model and compared using various linear contrasts to make inferences pertaining to seasonal prey selectivity. Results indicated spiders foraged selectively over the course of the study, contrary to predictions derived from optimal foraging theory. Even during winter, with overall low prey densities, the relative rates of predation compared to available prey differed significantly over time and by prey group. Moreover, these spiders appeared to diversify their diets; the least abundant prey group was consistently overrepresented in the diet within a given season. We suggest that foraging in generalist predators is not necessarily restricted to frequency dependency during winter. In fact, foraging motives other than energy maximization, such as a more nutrient‐focused strategy, may also be optimal for generalist predators during prey‐scarce winters.     

Constraints on prey size selection by the three-spined stickleback: energy requirements and the capacity and fullness of the gut

An experiment was designed to study how gut fullness and encounter with 5-mm Asellus aquaticus influenced acceptance or rejection of less profitable 8-mm Asellus . 45-mm sticklebacks were found to always accept 5-mm prey whereas 8-mm prey were accepted with an initial probability of about 0.9. This probability decreased as the gut filled. Fish of differing sizes and sex had similar daily energy intakes per unit body size, however the acceptance of 8-mm prey was related to fish size. Whenever a fish orientated to a prey it was followed by pursuit and manipulation independently of prey size. The decision to accept or reject prey occurred after one manipulation, a criterion that was more variable for the larger prey. For one feeding session per day the total energy intake was almost constant despite the changing combination of prey sizes eaten. The fish ate prey with long handling times if the energetic contents of the stomach had not reached 450 J. Calculations were made of how many of each millimetre prey size group would satisfy the 450 J demand and how long the estimated number would take to handle. This showed that the best option is to consume 5-mm prey if given the choice.     

Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species

1. In order to understand the relative importance of prey quality and mobility in indirect interactions among alternative prey that are mediated by a shared natural enemy, the nutritional quality of two common prey for a generalist insect predator along with the predator's relative preference for these prey was determined. 2. Eggs of the corn earworm Helicoverpa zea (Lepidoptera: Noctuidae) were nutritionally superior to pea aphids Acyrthosiphum pisum (Homoptera: Aphididae) as prey for big‐eyed bugs Geocoris punctipes (Heteroptera: Geocoridae). Big‐eyed bugs survived four times as long when fed corn earworm eggs than when fed pea aphids. Furthermore, only big‐eyed bugs fed corn earworm eggs completed development and reached adulthood. 3. In two separate choice experiments, however, big‐eyed bugs consistently attacked the nutritionally inferior prey, pea aphids, more frequently than the nutritionally superior prey, corn earworm eggs. 4. Prey mobility, not prey nutritional quality, seems to be the most important criterion used by big‐eyed bugs to select prey. Big‐eyed bugs attacked mobile aphids preferentially when given a choice between mobile and immobilised aphids. 5. Prey behaviour also mediated indirect interactions between these two prey species. The presence of mobile pea aphids as alternative prey benefited corn earworms indirectly by reducing the consumption of corn earworm eggs by big‐eyed bugs. The presence of immobilised pea aphids, however, did not benefit corn earworms indirectly because the consumption of corn earworm eggs by big‐eyed bugs was not reduced when they were present. 6. These results suggest that the prey preferences of generalist insect predators mediate indirect interactions among prey species and ultimately affect the population dynamics of the predator and prey species. Understanding the prey preferences of generalist insect predators is essential to predict accurately the efficacy of these insects as biological control agents.     

An order-specific monoclonal antibody to Diptera reveals the impact of alternative prey on spider feeding behavior in a complex food web

Generalist predators have the capacity to restrict pest population growth, especially early in the season before densities increase. However, their polyphagous feeding habits sometimes translate into reduced pest consumption when they target alternative prey. An order-specific monoclonal antibody was developed to examine the strength of trophic connections between Diptera, a major category of non-pest prey, and linyphiid spiders in alfalfa. We report the development and characterization of a monoclonal antibody with order-level specificity to Diptera. This antibody elicited strong absorbance to 22 Diptera from 13 families, no false-positive reactivity to non-dipteran invertebrates, and antigen detection periods following prey consumption that were comparable between spiders. Over 900 field-collected females of the linyphiid spiders Erigone autumnalis and Bathyphantes pallidus were screened for Diptera antigen. Significantly more B. pallidus screened positive for Diptera (40%) compared to E. autumnalis (16%), indicating differential reliance on these prey. In parallel with the collection of spiders for gut-content analysis, prey availability was estimated at web sites. The two spiders exhibited different feeding responses to prey availability. Consumption of Diptera by B. pallidus was strongly correlated with Diptera abundance whilst the availability of other potential prey did not influence predation rates. Conversely, E. autumnalis did not prey upon Diptera in proportion to availability, but increased Collembola activity-density reduced dipteran consumption. Integration of molecular gut-content analysis with precise sampling of prey demonstrated how two closely related linyphiid spiders exhibit different feeding responses to the availability of prey under natural field conditions. Elucidating the feeding preferences of natural enemies is critical to effective incorporation of biological control by generalist predators in the management of agricultural pests.     

Evolution of stenophagy in spiders (Araneae): evidence based on the comparative analysis of spider diets

Stenophagy (narrow diet breadth) represents an extreme of trophic specialization in carnivores, but little is known about the forces driving its evolution. We used spiders, the most diversified group of terrestrial predators, to investigate whether stenophagy (1) promoted diversification; (2) was phylogenetically conserved and evolutionarily derived state; and (3) was determined either by geographical distribution and foraging guild. We used published data on the prey of almost 600 species. Six categories of stenophagy were found: myrmecophagy, araneophagy, lepidopterophagy, termitophagy, dipterophagy, and crustaceophagy. We found that the species diversity of euryphagous genera and families was similar to stenophagous genera and families. At the family level, stenophagy evolved repeatedly and independently. Within families, the basal condition was oligophagy or euryphagy. Most types of stenophagy were clearly derived: myrmecophagy in Zodariidae; lepidopterophagy in Araneidae; dipterophagy in Theridiidae. In contrast, araneophagy was confined to basal and intermediate lineages, suggesting its ancestral condition. The diet breadth of species from the tropics and subtropics was less diverse than species from the temperate zone. Diet breadth was lower in cursorial spiders compared to web-building species. Thus, the evolution of stenophagy in spiders appears to be complex and governed by phylogeny as well as by ecological determinants.     

Pyrosequencing of prey DNA in reptile faeces: analysis of earthworm consumption by slow worms

Little quantitative ecological information exists on the diets of most invertebrate feeding reptiles, particularly nocturnal or elusive species that are difficult to observe. In the UK and elsewhere, reptiles are legally required to be relocated before land development can proceed, but without knowledge of their dietary requirements, the suitability of receptor sites cannot be known. Here, we tested the ability of non-invasive DNA-based molecular diagnostics (454 pyrosequencing) to analyse reptile diets, with the specific aims of determining which earthworm species are exploited by slow worms (the legless lizard Anguis fragilis) and whether they feed on the deeper-living earthworm species that only come to the surface at night. Slow worm faecal samples from four different habitats were analysed using earthworm-specific PCR primers. We found that 86% of slow worms (N=80) had eaten earthworms. In lowland heath and marshy/acid grassland, Lumbricus rubellus, a surface-dwelling epigeic species, dominated slow worm diet. In two other habitats, riverside pasture and calciferous coarse grassland, diet was dominated by deeper-living anecic and endogeic species. We conclude that all species of earthworm are exploited by these reptiles and lack of specialization allows slow worms to thrive in a wide variety of habitats. Pyrosequencing of prey DNA in faeces showed promise as a practical, rapid and relatively inexpensive means of obtaining detailed and valuable ecological information on the diets of reptiles.     

Prey selection by a spider wasp,Batozonellus lacerticida (Hymenoptera: Pompilidae): Effects of seasonal variation in prey species,size and density

Prey selection by a spider wasp,Batozonellus lacerticida, was investigated at the riverside of the Toyohira River in Misumai, Sapporo, Hokkaido over 7 years from 1981 to 1987. Seventeen species of araneid spiders were found in the study area and six of them were hunted by the wasps. Most (97.3%) of the 223 prey records obtained were of three species,Araneus macacus, A. marmoreus andA. pinguis. Nesting activity of the wasps continued until mid-August in 1981, 1982 and 1986, but stopped in July in 1984, 1985 and 1987. The length of nesting period was related to whether the wasps successfully switched prey species fromA. macacus toA. marmoreus andA. pinguis andA. pinguis or not Switching seemed to occur at the phase when density ofA. macacus remained high, depending on the density of largerA. marmorus andA. pinguis. This switching had large effects on species composition and size distribution of actual prey. Chesson's index α calculated at every 10 day period revealed that the wasps preferredA. macacus to the two other species and large prey to medium and small ones. The effect of prey density on preference depended on whetherA. macacus was present or absent. In the presence of it there were only slight differences in preference among various conditions of prey density. However, whenA. macacus was absent, densities of bothA. marmoreus andA. pinguis had some complementary effects on preference. The importance of prey size selection by pompilid wasps, and implications of density effects on preference are discussed.     

Development of an immunological technique for identifying multiple predator–prey interactions in a complex arthropod assemblage

A simplified but highly effective approach for the post‐mortem evaluation of predation on several targeted members of an arthropod assemblage that does not require the development of pest‐specific enzyme‐linked immunosorbent assay (ELISA) (e.g. pest‐specific monoclonal antibodies) or PCR assays (DNA primers) is described. Laboratory feeding studies were conducted to determine if predation events could be detected from predators that consumed prey marked with foreign protein. I determined that large and small rabbit immunoglobulin G (IgG)‐marked prey can be detected by a rabbit‐IgG‐specific ELISA in the guts of chewing and piercing–sucking type predators. I then conducted multifaceted inclusion and exclusion field cage studies to qualify the degree of interguild and intraguild predation occurring among a complex arthropod assemblage during four separate light phase treatments. The field cages contained an arthropod assemblage consisting of 11 or 12 species of predaceous arthropods and three pest species. The three pests introduced into the cages included third instar Trichoplusia ni marked with rabbit IgG, third instar Lygus hesperus marked with chicken IgG and Pectinophora gossypiella sentinel egg masses. The inclusion cages allowed foraging fire ants, Solenopis xyloni, to freely enter the cages while the exclusion cages contained barriers that prevented ant entry. The results obtained using the conventional inclusion/exclusion field cage methodology revealed that there was substantial interguild and intraguild predation occurring on the majority of the arthropods in the assemblage, particularly in those cages that included ants. I then precisely identified which predators in the assemblage were feeding on the three targeted pests by conducting three post‐mortem gut content analyses on each individual predator (1503 individuals) in the assemblage. Specifically, P. gossypiella egg predation events were detected using an established P. gossypiella‐egg‐specific ELISA, and third instar T. ni and L. hesperus predation events were detected using rabbit‐IgG‐specific and chicken‐IgG‐specific ELISAs, respectively. Generally, the gut ELISAs revealed that Collops vittatus, Spanagonicus albofasciatus and Geocoris punctipes readily preyed on P. gossypiella eggs; Nabis alternatus, Zelus renardii and spiders (primarily Misumenops celer) readily preyed on marked L. hesperus nymphs, and spiders, S. albofasciatus and N. alternatus readily preyed on T. ni larvae. Furthermore, the cage methods and the post‐mortem predator gut ELISAs revealed very few distinctive patterns of predation with regard to the light cycle the assemblage was exposed to.     

Electrophoretic analysis of the prey spectrum of Teretrius nigrescens (Lewis) (Col., Histeridae), a predator of Prostephanus truncatus (Horn) (Col., Bostrichidae), in Mexico, Honduras, and Benin

Abstract: Extensive collections of Teretrius nigrescens in Mexico, Honduras, and Benin, were electrophoretically analysed to elucidate the prey spectrum of the predator. Both polyacrylamide gel electrophoresis and cellulose acetate electrophoresis were used. Beetles were sampled with pheromone traps, using the synthetic aggregation pheromone of Prostephanus truncatus , and directly from farmers' maize stores. The proportion of electrophoretically detected prey protein from adult T. nigrescens in pheromone traps was low: of the 1108 specimens analysed, only in 34 cases, prey protein could be clearly identified. More frequently, prey protein was detected in adult T. nigrescens sampled in maize stores in Mexico, Honduras, and Benin, with 87 samples showing distinct prey bands of the total 1214 predators analysed. Of the 241 T. nigrescens larvae sampled in maize stores in Benin, 136 showed distinct bands of prey protein. In all samples, P. truncatus was the most frequently detected prey species. The second most often identified prey species was Sitophilus zeamais . The results are discussed with regard to various methods for prey spectrum analysis and specifically the biology of T. nigrescens .     

Effect of zooplankton type and abundance on prey consumption by the fairy shrimp, Streptocephalus proboscideus (Anostraca: Crustacea)

Laboratory cultured Streptocephalus proboscideus (three sizes (mm), viz. 8.44 ± 0.95 (virgin), 14.18 ± 1.49 (adult I) and 19.24 ± 1.52 (adult II)) were offered (separately for males and females) field collected zooplankton (12 prey types) at three levels of abundance (1.0 ml⁻¹, 2.0 ml⁻¹ and 4.1 ind. ml⁻¹ in 30-minute feeding experiments. Gut contents, analyzed for abundance and diversity of prey type, showed that predator size, sex and their interaction had strong effects on prey consumption. Regardless of their size, and of prey density, S. proboscideus females consumed 25–90% more prey than males. Their filtration rates (adult II) were higher (125 ml ind.⁻¹ h.⁻¹) than those of males (30 ml ind.⁻¹ h.⁻¹) too. Rotifers had the highest numerical percentage in the gut, regardless of predator size or sex. Cladocerans were only consumed by adults I and II. Adult II females consumed 28.5–43.3 μg zooplankton dry weight ind.⁻¹ h.⁻¹. Size distribution of B. longirostris in the field and in the gut were closely similar. This study confirms S. proboscideus as a non-selective filter feeder. Since it did not eat jumping rotifers, copepod nauplii and copepodites, it may contribute to structuring its prey communities, because good escapers will be enriched in the medium, while poor escapers will be depleted.     

The influence of time and temperature on molecular gut content analysis： Adalia bipunctata fed with Rhopalosiphum padi

Gut content analysis is a useful tool when studying arthropod predator-prey interactions. We used polymerase chain reaction （PCR） technique to examine how detection of prey DNA in the gut content of predators was influenced by digestion time and temperature. Such knowledge is critical before applying PCR-based gut content analysis to field collected predators. Larvae of the two-spotted ladybeetle （Adalia bipunctata L.） were fed with the bird cherry-oat aphid （Rhopalosiphum padi L.） at either 21℃ or 14℃. After consuming one aphid, the predators were allowed to digest the prey for a range of time periods up to 24 hours. The influence of temperature on A. bipunctata feeding behavior was also recorded. From the fed larvae, total DNA was extracted and PCR reactions with R. padi specific primers were run. The number ofA. bipunctata that tested positive for R. padi DNA was negatively related to the length of digestion time. Temperature influenced larval feeding behavior but did not have a significant effect on R. padi DNA detection. After pooling the data from both temperature treatments we estimated the time point when R. padi DNA could be amplified from 50% of the fed A. bipunctata by PCR to be 4.87 hours. With such a rapid decrease in prey DNA detection success, positive PCR reactions will most likely be the result of predation events occurring shortly before capture. If a defined digestion temperature range has proven not to influence prey detection, PCR data obtained from predators collected within that particular range can be interpreted in the same way.     

An immunological approach to quantify consumption of protein-tagged Lygus hesperus by the entire cotton predator assemblage

A new method for post-mortem quantification of predation on prey items marked with protein antigens is described. First, short-term protein marking retention tests were conducted on the targeted prey, immature Lygus hesperus Knight (Heteroptera: Miridae). Chicken IgG, rabbit IgG, or soy milk proteins were readily detectable by a suite of protein specific enzyme-linked immunosorbent assays (ELISA) on the L. hesperus. Then, predator gut content assays were conducted on chewing and piercing–sucking type predators that consumed a 3rd instar L. hesperus marked with rabbit IgG. The rabbit IgG gut content ELISA detected the marked prey in the vast majority of both types of predators for up to 24 h after feeding. Finally, field cage studies were conducted to quantify predation rates of the natural cotton predator assemblage on protein marked L. hesperus nymphs. Each 4th instar L. hesperus marked with rabbit IgG, chicken IgG, and soy milk was released into one of 360 field cages containing a cotton plant and the natural population of predators. After 7 h, each caged plant was pulled from the field, the number of predaceous arthropods in each cage were tallied, and each individual predator was assayed for the presence of marked prey by a suite of protein-specific ELISAs. A procedural error with the soy mark application negated the anti-soy ELISA data, but the anti-rabbit IgG and anti-chicken IgG ELISAs pinpointed exactly which predators preyed on the IgG marked nymphs. The protein-specific gut ELISAs revealed that various members of Araneae, Heteroptera, and Coleoptera were the most common predators of the marked prey items. In all, 74 predation events were recorded in the guts of the 556 predators encountered in the field cages. Of these 26, 23, and 14 marked individuals were eaten by various members of Araneae, Heteroptera, and Coleoptera, respectively. This study verifies that prey immunomarking is a simple, versatile, and effective method for quantifying predation rates on L. hesperus.     

Control of aphids on wheat by generalist predators: effects of predator density and the presence of alternative prey

There is evidence for both positive and negative effects of generalist predators on pest populations and the various reasons for these contrasting observations are under debate. We studied the influence of a generalist predator, Pardosa lugubris (Walckenaer) (Araneae: Lycosidae), on an aphid pest species, Rhopalosiphum padi (L.) (Hemiptera: Aphididae; low food quality for the spider), and its host plant wheat, Triticum spec. (Poaceae). We focused on the role of spider density and the availability of alternative prey, Drosophila melanogaster Meigen (Diptera: Drosophilidae; high food quality). The presence of spiders significantly affected plant performance and aphid biomass. Alternative prey and spider density strongly interacted in affecting aphids and plants. High spider density significantly improved plant performance but also at low spider density plants benefited from spiders especially in the presence of alternative prey. The results suggest that generalist arthropod predators may successfully reduce plant damage by herbivores. However, their ability to control prey populations varies with predator nutrition, the control of low-quality prey being enhanced if alternative higher-quality prey is available.     

Effects of prey aphid species on the abundance of a parasitoid and two predator species in aphid colonies attended by ants on citrus

This study focused on three species of enemies, the parasitoid wasp Lysiphlebus japonicus Ashmead (Hymenoptera: Aphidiidae), the ladybird Scymnus posticalis Sicard (Coleoptera: Coccinellidae) and the predatory gall midge Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae), all of which are able to exploit aphids attended by ants. I experimentally evaluated the effects of prey aphid species on the abundance of each of the three enemy species in ant‐attended aphid colonies on citrus. The aphids compared were Aphis gossypii Glover versus Aphis spiraecola Patch in late spring, and Toxoptera citricidus (Kirkaldy) versus A. spiraecola in late summer (all, Hemiptera: Aphididae). Colonies of the three aphid species were attended by the ant Pristomyrmex punctatus Smith (Hymenoptera: Formicidae). The initial number of attending ants per individual aphid did not differ significantly between the colonies of the two aphid species compared in each season. Between A. gossypii and A. spiraecola, there was no significant difference in the number of mummies formed by the parasitoid or foraging larvae of each of the two predators per aphid colony. A significant difference was detected between T. citricidus and A. spiraecola for each of the three enemy species, with a far greater number of L. japonicus mummies in T. citricidus colonies and distinctly more larvae of each of the two predators in A. spiraecola colonies. Thus, the abundance of each of the three enemy species in ant‐attended aphid colonies was significantly influenced by the species of the prey aphids, with the three enemies showing different responses to the three aphid species.