James R. Bell

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.

Phenological sensitivity to climate across taxa and trophic levels

Differences in phenological responses to climate change among species can desynchronise ecological interactions and thereby threaten ecosystem function. To assess these threats, we must quantify the relative impact of climate change on species at different trophic levels. Here, we apply a Climate Sensitivity Profile approach to 10,003 terrestrial and aquatic phenological data sets, spatially matched to temperature and precipitation data, to quantify variation in climate sensitivity. The direction, magnitude and timing of climate sensitivity varied markedly among organisms within taxonomic and trophic groups. Despite this variability, we detected systematic variation in the direction and magnitude of phenological climate sensitivity. Secondary consumers showed consistently lower climate sensitivity than other groups. We used mid-century climate change projections to estimate that the timing of phenological events could change more for primary consumers than for species in other trophic levels (6.2 versus 2.5–2.9 days earlier on average), with substantial taxonomic variation (1.1–14.8 days earlier on average).

Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community

Insect parasitoids play a major role in terrestrial food webs as they are highly diverse, exploit a wide range of niches and are capable of affecting host population dynamics. Formidable difficulties are encountered when attempting to quantify host–parasitoid and parasitoid–parasitoid trophic links in diverse parasitoid communities. Here we present a DNA‐based approach to effectively track trophic interactions within an aphid–parasitoid food web, targeting, for the first time, the whole community of parasitoids and hyperparasitods associated with a single host. Using highly specific and sensitive multiplex and singleplex polymerase chain reaction, endoparasitism in the grain aphid Sitobion avenae (F) by 11 parasitoid species was quantified. Out of 1061 aphids collected during 12 weeks in a wheat field, 18.9% were found to be parasitized. Parasitoids responded to the supply of aphids, with the proportion of aphids parasitized increasing monotonically with date, until the aphid population crashed. In addition to eight species of primary parasitoids, DNA from two hyperparasitoid species was detected within 4.1% of the screened aphids, with significant hyperparasitoid pressure on some parasitoid species. In 68.2% of the hyperparasitized aphids, identification of the primary parasitoid host was also possible, allowing us to track species‐specific parasitoid‐hyperparasitoid links. Nine combinations of primary parasitoids within a single host were found, but only 1.6% of all screened aphids were multiparasitized. The potential of this approach to parasitoid food web research is discussed.

Prey choice by carabid beetles feeding on an earthworm community analysed using species- and lineage-specific PCR primers

The carabid beetle Pterostichus melanarius is a major natural enemy of pests, such as aphids and slugs in agricultural systems. Earthworms are a dominant non‐pest component of the diet of P. melanarius which help sustain the beetles during periods when the pest population is low or absent. In this study we wanted to test whether this predator exercises prey choice among different earthworm species or ecological groups. High levels of genetic diversity within morphological species of earthworm necessitated the development of primers that were specific not just to species but lineages and sub‐lineages within species as well. Gut samples from beetles were analysed using multiplex‐PCR and fluorescent‐labelled primers. Calibratory feeding trials were undertaken to calculate median detection times for prey DNA following ingestion. Extensive testing demonstrated that the primers were species‐specific, that detection periods were negatively related to amplicon size and that meal size had a highly significant effect on detection periods. Monte Carlo simulations showed that, in general, worms were being predated in proportion to their densities in the field with little evidence of prey choice, other than probable avoidance of the larger, deep‐living species. There was no evidence that epigeic species were being taken preferentially in comparison with endogeic species. There was also no evidence that defensive secretions by Allolobophora chlorotica reduced predation pressure on this species by P. melanarius. We concluded that any management system that increases earthworm densities generally, regardless of component species, is likely to be optimal for increasing numbers of this beneficial beetle predator.

Handbook of protocols for standardized measurement of terrestrial invertebrate functional traits

Summary 1. Trait-based approaches are increasingly being used to test mechanisms underlying species assemblages and biotic interactions across a wide range of organisms including terrestrial arthropods and to investigate consequences for ecosystem processes. Such an approach relies on the standardized measurement of functional traits that can be applied across taxa and regions. Currently, however, unified methods of trait measurements are lacking for terrestrial arthropods and related macroinvertebrates (terrestrial invertebrates hereafter). 2. Here, we present a comprehensive review and detailed protocol for a set of 29 traits known to be sensitive to global stressors and to affect ecosystem processes and services. We give rec- ommendations how to measure these traits under standardized conditions across various ter- restrial invertebrate taxonomic groups. 3. We provide considerations and approaches that apply to almost all traits described, such as the selection of species and individuals needed for the measurements, the importance of intraspecific trait variability, how many populations or communities to sample and over which spatial scales. 4. The approaches outlined here provide a means to improve the reliability and predictive power of functional traits to explain community assembly, species diversity patterns and ecosystem processes and services within and across taxa and trophic levels, allowing compar- ison of studies and running meta-analyses across regions and ecosystems. 5. This handbook is a crucial first step towards standardizing trait methodology across the most studied terrestrial invertebrate groups, and the protocols are aimed to balance general applicability and requirements for special cases or particular taxa. Therefore, we envision this handbook as a common platform to which researchers can further provide methodological input for additional special cases.

Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation

Generalist predators and parasitoids are considered to be important regulators of aphids. The former not only feed on these pests, but might also consume parasitoids at all stages of development. This direct or coincidental interference affects the natural control of aphids, the scale of which is largely unknown, and it has rarely been examined under natural conditions. Here, molecular diagnostics were used to track trophic interactions in an aphid-parasitoid-generalist predator community during the build-up of a cereal aphid population. We found that generalist predators, principally carabid and staphylinid beetles as well as linyphiid spiders, had strong trophic links to both parasitoids and aphids. Remarkably, more than 50% of the parasitoid DNA detected in predators stems from direct predation on adult parasitoids. The data also suggest that coincidental intraguild predation is common too. Generalist predators, hence, disrupt parasitoid aphid control, although the levels at which the predators feed on pests and parasitoids seem to vary significantly between predator taxa. Our results suggest that taxon-specific trophic interactions between natural enemies need to be considered to obtain a more complete understanding of the route to effective conservation biological control.

Seasonal migration to high latitudes results in major reproductive benefits in an insect

Little is known of the population dynamics of long-range insect migrants, and it has been suggested that the annual journeys of billions of nonhardy insects to exploit temperate zones during summer represent a sink from which future generations seldom return (the “Pied Piper” effect). We combine data from entomological radars and ground-based light traps to show that annual migrations are highly adaptive in the noctuid moth Autographa gamma (silver Y), a major agricultural pest. We estimate that 10–240 million immigrants reach the United Kingdom each spring, but that summer breeding results in a fourfold increase in the abundance of the subsequent generation of adults, all of which emigrate southward in the fall. Trajectory simulations show that 80% of emigrants will reach regions suitable for winter breeding in the Mediterranean Basin, for which our population dynamics model predicts a winter carrying capacity only 20% of that of northern Europe during the summer. We conclude not only that poleward insect migrations in spring result in major population increases, but also that the persistence of such species is dependent on summer breeding in high-latitude regions, which requires a fundamental change in our understanding of insect migration.

Intraguild predation in winter wheat: prey choice by a common epigeal carabid consuming spiders

Predators can provide a valuable ecosystem service by suppressing crop pests. However, intraguild predation, where predators compete for the same prey resource whilst consuming each other, may destabilize population dynamics and increase the risk of pest outbreaks. Very little is known about intraguild predation in open fields or the strengths of trophic links between predators which may negatively affect pest control. We tested the null hypothesis that predation by the epigeal predator Pterostichus melanarius (Coleoptera: Carabidae) on different spiders is species-independent (proportional to density). A combination of population monitoring in winter wheat, molecular identification of juvenile spiders, molecular analysis of predator gut contents and a Monte Carlo simulation model were used to analyse prey choice. Pterostichus melanarius were pitfall-trapped over three months, and 622 individuals were screened for the remains of four spider species. Predation rates on spiders were 43·6% in June and 33·3% in August and showed clear evidence of prey choice. Predation on the web-dependent Tenuiphantes tenuis (Linyphiidae) was significantly greater than predicted from a random choice model, while predation on Bathyphantes gracilis (Linyphiidae) was significantly lower. The beetles may be selecting the most abundant species disproportionately (switching) or responding in some cases to spatial niche separation (T. tenuis locate their webs marginally lower than B. gracilis). However, two itinerant hunters, Erigone spp. (Linyphiidae) and Pachygnatha degeeri (Tetragnathidae), were consumed in proportion to their density. Synthesis and applications. High levels of intraguild predation were revealed using molecular diagnostics. The gut analysis approach provided invaluable data that will inform the future design of appropriate pest management and integrated farming strategies that encourage these predators. The data showed strong evidence of prey choice. Managers can, however, probably encourage high densities of all these known aphid predators (spiders and carabids) because disproportionately high rates of predation on the most common spiders at our field sites (T. tenuis) were not sufficient to prevent strong growth in the density of this species between June and August (adults increased × 1·6 and juveniles × 8·6). Such work is essential if we are to reveal the processes behind functional biodiversity in crops.

Spider communities as tools in monitoring reclaimed limestone quarry landforms

Spider communities are sensitive to a wide range of environmental factors and are potential ecological indicators which may be effective in the assessment and monitoring of restored ecosystems. One restoration technique of disused limestone quarry faces, landform replication, attempts to create landforms and ecosystems similar to those found on natural dalesides. Vegetation surveys indicate that communities developing on landform replications are more closely allied to natural dalesides than are those of naturally recolonised disused quarries. Assessment of the spider communities of three landform replication sites, a natural limestone daleside and seven naturally recolonised disused limestone quarries, using DECORANA and TWINSPAN, produced differing patterns of sites than those observed through the assessment of the vegetation communities. DECORANA assessment based on vascular plant species composition highlights the similarities between daleside and reclaimed site communities. The sensitivity of spider communities to vegetation structure and extent of bare ground highlights differences between sites and provides evidence of important differences in vegetation community development particularly in relation to cover and structure. Implications for the assessment of reclamation and restoration techniques are discussed.

Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids

1. Aphids represent a significant challenge to food production. The Rothamsted Insect Survey (RIS) runs a network of 12·2-m suction-traps throughout the year to collect migrating aphids. In 2014, the RIS celebrated its 50th anniversary. This paper marks that achievement with an extensive spatiotemporal analysis and the provision of the first British annotated checklist of aphids since 1964. 2. Our main aim was to elucidate mechanisms that advance aphid phenology under climate change and explain these using life-history traits. We then highlight emerging pests using accumulation patterns. 3. Linear and nonlinear mixed-effect models estimated the average rate of change per annum and effects of climate on annual counts, first and last flights and length of flight season since 1965. Two climate drivers were used: the accumulated day degrees above 16 °C (ADD16) indicated the potential for migration during the aphid season; the North Atlantic Oscillation (NAO) signalled the severity of the winter before migration took place. 4. All 55 species studied had earlier first flight trends at rate of β = −0·611 ± SE 0·015 days year−1. Of these species, 49% had earlier last flights, but the average species effect appeared relatively stationary (β = −0·010 ± SE 0·022 days year−1). Most species (85%) showed increasing duration of their flight season (β = 0·336 ± SE 0·026 days year−1), even though only 54% increased their log annual count (β = 0·002 ± SE <0·001 year−1). 5. The ADD16 and NAO were shown to drive patterns in aphid phenology in a spatiotemporal context. Early in the year when the first aphids were migrating, the effect of the winter NAO was highly significant. Further into the year, ADD16 was a strong predictor. Latitude had a near linear effect on first flights, whereas longitude produced a generally less-clear effect on all responses. Aphids that are anholocyclic (permanently parthenogenetic) or are monoecious (non-host-alternating) were advancing their phenology faster than those that were not. 6. Climate drives phenology and traits help explain how this takes place biologically. Phenology and trait ecology are critical to understanding the threat posed by emerging pests such as Myzus persicae nicotianae and Aphis fabae cirsiiacanthoidis, as revealed by the species accumulation analysis.