Do functional traits improve prediction of predation rates for a disparate group of aphid predators?

Aphid predators are a systematically disparate group of arthropods united on the basis that they consume aphids as part of their diet. In Europe, this group includes Araneae, Opiliones, Heteroptera, chrysopids, Forficulina, syrphid larvae, carabids, staphylinids, cantharids and coccinellids. This functional group has no phylogenetic meaning but was created by ecologists as a way of understanding predation, particularly for conservation biological control. We investigated whether trait-based approaches could bring some cohesion and structure to this predator group. A taxonomic hierarchy-based null model was created from taxonomic distances in which a simple multiplicative relationship described the Linnaean hierarchies (species, genera, etc.) of fifty common aphid predators. Using the same fifty species, a functional groups model was developed using ten behavioural traits (e.g. polyphagy, dispersal, activity, etc.) to describe the way in which aphids were predated in the field. The interrelationships between species were then expressed as dissimilarities within each model and separately analysed using PROXSCAL, a multidimensional scaling (MDS) program. When ordinated using PROXSCAL and then statistically compared using Procrustes analysis, we found that only 17% of information was shared between the two configurations. Polyphagy across kingdoms (i.e. predatory behaviour across animal, plant and fungi kingdoms) and the ability to withstand starvation over days, weeks and months were particularly divisive within the functional groups model. Confirmatory MDS indicated poor prediction of aphid predation rates by the configurations derived from either model. The counterintuitive conclusion was that the inclusion of functional traits, pertinent to the way in which predators fed on aphids, did not lead to a large improvement in the prediction of predation rate when compared to the standard taxonomic approach.

Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators.

Predation by generalist predators is difficult to study in the field because of the complex effects of positive and negative interactions within and between predator species and guilds. Predation can be monitored by molecular means, through identification of prey DNA within predators. However, polymerase chain reaction (PCR) amplification of prey DNA from predators cannot discriminate between primary and secondary predation (hyperpredation), in which one predator feeds on another that has recently eaten the target prey. Here we quantify, for the first time, the potential error caused by detection of prey DNA following secondary predation, using an aphid-spider-carabid model. First, the aphid Sitobion avenae was fed to the spider Tenuiphantes tenuis and the carabid Pterostichus melanarius, and the postconsumption detection periods, for prey DNA within predators, were calculated. Aphids were then fed to spiders and the spiders to carabids. Aphid DNA was detected in the predators using primers that amplified 245- and 110-bp fragments of the mitochondrial cytochrome oxidase I gene. Fragment size and predator sex had no significant effect on detection periods. Secondary predation could be detected for up to 8 h, when carabids fed on spiders immediately after the latter had consumed aphids. Beetles tested positive up to 4 h after eating spiders that had digested their aphid prey for 4 h. Clearly, the extreme sensitivity of PCR makes detection of secondary predation more likely, and the only reliable answer in future may be to use PCR to identify, in parallel, instances of intraguild predation.

Monoclonal antibodies reveal the potential of the tetragnathid spider Pachygnatha degeeri (Araneae: Tetragnathidae) as an aphid predator.

The drive towards a more sustainable and integrated approach to pest management has engendered a renewed interest in conservation biological control, the role of natural enemy communities and their interactions with prey. Monoclonal antibodies have provided significant advances in enhancing our knowledge of trophic interactions and can be employed to help quantify predation on target species. The tetragnathid spider Pachygnatha degeeri Sundevall was collected from fields of winter wheat in the UK and assayed by ELISA for aphid proteins. It was demonstrated that this spider did not simply consume greater quantities of aphids because it was bigger. In addition, P. degeeri contained significantly greater concentrations of aphid in their guts than other spiders, showing that aphids comprised a greater proportion of their diet. Although P. degeeri constituted only 6% of the spider population numerically, females and males respectively contained 16% and 37% of total aphid proteins within all spiders screened, significantly more than their density would predict. These spiders also preyed upon aphids at a disproportionately high rate in June, during the aphid establishment phase, theoretically the best time for limiting growth in the aphid population. Although less abundant than other generalist predators, the capability of these hunting spiders to consume large numbers of aphids highlights them as a more significant component of the predator complex than had previously been realized. Limitation of aphid numbers early in the year by generalist predators provides more time for the specialist aphid predators and parasitoids to move in.

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.

Study of temperature-growth interactions of entomopathogenic fungi with potential for control of Varroa destructor (Acari: Mesostigmata) using a nonlinear model of poikilotherm development.

AIMS: To investigate the thermal biology of entomopathogenic fungi being examined as potential microbial control agents of Varroa destructor, an ectoparasite of the European honey bee Apis mellifera. METHODS AND RESULTS: Colony extension rates were measured at three temperatures (20, 30 and 35 degrees C) for 41 isolates of entomopathogenic fungi. All of the isolates grew at 20 and 30 degrees C but only 11 isolates grew at 35 degrees C. Twenty-two isolates were then selected on the basis of appreciable growth at 30-35 degrees C (the temperature range found within honey bee colonies) and/or infectivity to V. destructor, and their colony extension rates were measured at 10 temperatures (12.5-35 degrees C). This data were then fitted to Schoolfield et al. [J Theor Biol (1981)88:719-731] re-formulation of the Sharpe and DeMichele [J Theor Biol (1977)64:649-670] model of poikilotherm development. Overall, this model accounted for 87.6-93.9% of the data variance. Eleven isolates exhibited growth above 35 degrees C. The optimum temperatures for extension rate ranged from 22.9 to 31.2 degrees C. Only three isolates exhibited temperature optima above 30 degrees C. The super-optimum temperatures (temperature above the optimum at which the colony extension rate was 10% of the maximum rate) ranged from 31.9 to 43.2 degrees C. CONCLUSIONS: The thermal requirements of the isolates examined against V. destructor are well matched to the temperatures in the broodless areas of honey bee colonies, and a proportion of isolates, should also be able to function within drone brood areas. SIGNIFICANCE AND IMPACT OF THE STUDY: Potential exists for the control of V. destructor with entomopathogenic fungi in honey bee colonies. The methods employed in this study could be utilized in the selection of isolates for microbial control prior to screening for infectivity and could help in predicting the activity of a fungal control agent of V. destructor under fluctuating temperature conditions.

Can generalist predators be effective biocontrol agents?

Theoretical developments are helping us to comprehend the basic parameters governing the dynamics of the interactions between generalist predators and their many pest and nonpest prey. In practice, however, inter- and intraspecific interactions between generalist predators, and between the predators and their prey, within multispecies systems under the influence of rapidly changing biotic and abiotic variables are difficult to predict. We discuss trade-offs between the relative merits of specialists and generalists that allow both to be effective, and often complementary, under different circumstances. A review of manipulative field studies showed that in approximately 75% of cases, generalist predators, whether single species or species assemblages, reduced pest numbers significantly. Techniques for manipulating predator numbers to enhance pest control at different scales are discussed. We now need to find ways of disentangling the factors influencing positive and negative interactions within natural enemy communities in order to optimize beneficial synergies leading to pest control.

Secondary predation: quantification of food chain errors in an aphid-spider-carabid system using monoclonal antibodies.

"Secondary predation" occurs when one predator feeds on a second predator, which has in turn eaten a target prey. Detection of prey remains within predators using monoclonal antibodies cannot distinguish between primary and secondary predation, potentially leading to quantitative and qualitative food chain errors. We report the first fully replicated experiments to measure secondary predation effects, using an aphid-spider-carabid system. Aphids, Sitobion avenae, were fed to spiders, Lepthyphantes tenuis, which were allowed to digest their prey for a range of time intervals. The spiders were then fed to carabids, Poecilus (=Pterostichus) cupreus, which were again allowed to digest their prey for set periods. The anti-aphid monoclonal antibody used to identify S. avenae remains in P. cupreus was one that detected an epitope that increased in availability over the first few hours of digestion, amplifying the signal, extending detection periods and thus increasing the chances of detecting secondary predation. Despite this, and the fact that spiders are known to digest their prey more slowly than many other predators, detection of secondary predation was only possible if the carabids were killed immediately after consuming at least two spiders which were, in turn, eaten immediately after consuming aphids. As this scenario is unlikely to occur frequently in the field it was concluded that secondary predation is unlikely to be a serious source of error during field studies.

Ecology and behavior of ground beetles (Coleoptera: Carabidae).

The ground beetles from the speciose beetle family Carabidae and, since their emergence in the Tertiary, have populated all habitats except deserts. Our knowledge about carabids is biased toward species living in north-temperate regions. Most carabids are predatory, consume a wide range of food types, and experience food shortages in the field. Feeding on both plant and animal material and scavenging are probably more significant than currently acknowledged. The most important mortality sources are abiotic factors and predators; pathogens and parasites can be important for some developmental stages. Although competition among larvae and adults does occur, the importance of competition as a community organization is not proven. Carabids are abundant in agricultural fields all over the world and may be important natural enemies of agricultural pests.

Do seasonal changes in numbers of aerially dispersing spiders reflect population density on the ground or variation in ballooning motivation?

Groups of linyphiid spiders (Erigone spp.) (Araneae, Linyphiidae), collected at intervals from arable land, were tested in laboratory bioassays to determine the proportion of individuals that exhibited ballooning behaviour on each field sampling occasion. There was no significant variation in the proportions of spiders in each test group ballooning in the laboratory over a year. Investigations of ground density and aerial dispersal, in a grass field and a winter-wheat field, confirmed that peaks in numbers of spiders observed ballooning in the field generally coincided with population peaks in the summer and autumn. Significant correlations between ground populations and aerial catches were found for total spiders, immature spiders, and Bathyphantes gracilis (Blackwall) in both fields, adult spiders in the grass field, Erigone spp. in the grass, and Meioneta rurestris (C.L. Koch) in the wheat. The other groups analysed, Lepthyphantes tenuis (Blackwall) in both fields, Erigone spp. in wheat, and M. rurestris in grass, showed similar but non-significant trends. No significant difference was found between overall ground-to-air ratios for males compared to females, but adult spiders were more likely to balloon than immatures.