Prey‐specific foraging tactics in a web‐building spider

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Diversity of spiders after spring sowing – influence of farming system and habitat type

Spiders contribute considerably to diversity in agroecosystems and are important components of natural pest control. Farming system and adjacent habitats may influence spider diversity. In this study, diversity of the spider families Lycosidae and Linyphiidae was studied after spring sowing until the time when a common pest (Rhopalosiphum padi) colonizes cereal fields. The spiders were collected with pitfall traps at eight organically or conventionally managed farms around Uppsala, Sweden, in three different habitats at each site: field margin, crop field and the edge between the two. The effects of farming system and habitat type on diversity of lycosids and linyphiids were considered using three different measures (activity density, species richness and composition). The most dominant species of each spider family, Pardosa agrestis (Lycosidae) and Oedothorax apicatus (Linyphiidae), had higher activity density at organic sites, and farming systems also contained different species compositions of both lycosid and linyphiid spiders. Also, linyphiid species richness was higher on conventional sites and linyphiid species composition was influenced by habitat type, in contrast with lycosids. Activity density and species richness of lycosid spiders were, on the other hand, more associated with field margins than linyphiid spiders.     

Tracking aphid predation by lycosid spiders in spring-sown cereals using PCR-based gut-content analysis

Detection of prey DNA-remains in arthropod predators by polymerase chain reaction (PCR) is useful when investigating food webs. In this study we estimated how long after a feeding event it was possible to detect mitochondrial COII DNA (331 bp) from an important aphid pest, Rhopalosiphum padi (Homoptera: Aphididae), in spiders of the genus Pardosa (Araneae: Lycosidae). Following laboratory evaluations we tested spiders collected in spring-sown cereals for aphid predation during two seasons. Aphids were digested rapidly in laboratory-fed predators and the time point when prey DNA could be amplified from 50% of the spiders was estimated to be 3.7 h. A total of 372 field- collected predators were analyzed by PCR and despite low aphid densities many spiders (26% in 2004 and 19% in 2005) tested positive for R. padi, indicating consumption of at least one aphid within a few hours before capture. The percentage of spiders that tested positive for R. padi DNA varied considerably between fields and logistic regression analysis revealed that the probability of detecting aphid DNA was significantly influenced by location and year. We conclude that Pardosa spiders, under certain conditions, frequently feed on R. padi and deserve special attention in conservation biological control.     

Web-site selection strategies of linyphiid spiders in alfalfa: implications for biological control

Site-specific foraging can enhance the ability of generalist predators to provide effective and sustainable levels of pest control in agroecosystems. This can result from increased growth rates, higher population densities, and improved capture frequencies of pests at high prey density microsites. We tested the hypothesis that linyphiid spiders would exhibit microhabitat-specific web-site selection strategies in alfalfa. This was predicted to result in high prey densities at web-sites compared to paired non-web-sites through direct, or indirect, selection of prey-rich habitats. A total of 22,242 potential prey items were collected from mini-sticky traps located at 896 microsites. Web-centered mini-sticky traps on the ground, representative of Erigone autumnalis Emerton (Araneae: Linyphiidae) webs, captured similar numbers of potential prey as paired non-web-centered traps nearby. However, aerial sticky traps at web-sites of Bathyphantes pallidus (Banks) (Araneae: Linyphiidae) contained significantly more Diptera and Empoasca fabae (Harris) (Homoptera: Cicadellidae) than paired non-web-centered sticky-traps. Prey activity-densities also varied between web-sites of E. autumnalis and B. pallidus. Diptera were dominant at aerial microsites of B. pallidus whilst Collembola were abundant on ground-based traps of E. autumnalis. These results suggest that in alfalfa, the pressure for selecting prey-rich web-sites by erigonine spiders is low, but B. pallidus exhibits a selective web-location strategy targeted towards high quality dipteran prey. These sites also captured large numbers of E. fabae, a major pest of alfalfa, thus implicating aerial-based linyphiines as valuable predators in biological control.     

Microcosm studies on control of aphids by generalist arthropod predators: Effects of alternative prey

Generalist predators are potential controlagents of aphids in cereal fields. Becauseaphids are low-quality prey for most generalistpredators, the availability of alternativehigh-quality prey may influence theinteractions between aphids and their predatorsby reducing the predation rate due to loweredpreference for aphids. We analysed this bytesting the ability of six generalist predators(the spiders Erigone atra (Bl.), Clubiona lutescens (Westr.)/reclusaO.P.-C., Pachygnatha degeeri Sundevall,Pardosa prativaga (L.Koch), the carabidbeetle Bembidion lampros (Herbst), andthe harvestman Oligolophus tridens (C.L.Koch)) to suppress Rhopalosiphum padi(Linné) populations in the presence orabsence of alternative prey types (fruit fliesDrosophila melanogaster (Meigen) or thecollembolan Tomocerus bidentatus(Folsom)). Experiments of 10 days duration werecarried out in a microcosm set-up. Withoutalternative prey all predators except B.lampros were able to reduce aphid populationdevelopment significantly relative topredator-free controls. The harvest spider O. tridens was the most efficient predator(<90% reduction). Presence of alternativeprey (fruit flies) had a significant negativeeffect on aphid limitation by P. prativagaand a weak positive effect in B. lampros, but did not influence the ability to reduce aphids in E. atra, Clubiona, P. degeeri and O. tridens. In addition, 24-hours' consumption experiments with adult P. degeeri and subadult C. lutescens/reclusa, using R. padi and D. melanogaster as prey types, showed markedly lower consumption rates of aphid than of fruit fly prey. The microcosm arrangement is a simple way to partly simulate the habitat complexity of an agricultural field under laboratory conditions and proved to be a useful tool for investigating complex predator-prey interactions.     

Spiders from multiple functional guilds are exposed to Bt-endotoxins in transgenic corn fields via prey and pollen consumption

A comprehensive assessment of risk to natural enemies from Bt-endotoxins from bioengineered crops must evaluate potential harm, as well as exposure pathways in non-target arthropod food webs. Despite being abundant generalist predators in agricultural fields, spiders (Araneae) have often been overlooked in the context of Bt crop risk assessment. Spiders and their prey were collected from transgenic corn fields expressing lepidopteran-specific Cry1Ab, coleopteran-specific Cry3Bb1, both proteins, and a non-transgenic near isoline. Spiders and prey were screened for Cry1Ab and Cry3Bb1 using qualitative enzyme-linked immunosorbent assay. Spiders from the three most common functional guilds, wandering sheet-tangle weavers, orb-weavers, and ground runners, tested positive for Cry1Ab and Cry3Bb1 proteins, with the highest per cent positive (8.0% and 8.3%) during and after anthesis. Laboratory feeding trials revealed that Bt-endotoxins were detectable in the Pardosa sp. (Lycosidae)-immature cricket-Bt corn pathway, but not in the Tennesseellum formica (Linyphiidae)-Collembola-Bt corn pathway. Additionally, direct consumption of transgenic corn pollen by Pardosa sp., T. formica, and Cyclosa turbinata (Araneidae) resulted in transfer of both Cry1Ab and Cry3Bb1 endotoxins. This study demonstrates that Bt-endotoxins are taken up by diverse members of a spider community via pollen and prey consumption and should be factored into future risk assessment.     

The value of three cereal aphid species as food for a generalist predator

The value of the cereal aphid species Metopolophium dirhodum (Wlk.), Sitobion avenae (F.) and Rhopalosiphum padi (L.) as prey for the linyphiid spider Erigone atra (Bl.) was assessed. Fecundity of females was determined for spiders fed on eight experimental diets: three single‐species aphid diets, a mixed diet of all three aphid species, three mixed diets with each aphid species in combination with fruit flies Drosophila melanogaster (Meig.), and pure D. melanogaster as a high quality comparison diet. The development and survival of first‐instar juveniles fed on three diets of single aphid species, and on a diet of Collembola were compared with those subjected to starvation. Prey value for adult females was assessed by egg production, hatching success and offspring size. In pure diets all three aphid species were of low value to the spiders, causing a rapid decline in egg production and supporting no growth of significance of first‐instar juveniles. No difference in value of aphid species of single‐species aphid diets was found in the fecundity experiment, while a ranking of aphid species of M. dirhodum > R. padi > S. avenae was revealed in the survivorship experiment. A mixed‐aphid diet was not found to be advantageous compared with single‐species aphid diets, and no advantage of including aphids in mixed diets with fruit flies was found. Metopolophium dirhodum and R. padi were neutral in mixed diets, while a diet of S. avenae and fruit flies caused reduced egg production compared with the pure diet of fruit flies, revealing a toxic effect of S. avenae on the spider. The value‐ranking of aphid species in mixed diets was similar to that of single‐species diets. A similar ranking of aphid species was found for different fitness parameters (fecundity of adult females and development of juveniles). A ranking of aphids by offspring size of mothers on aphid‐only diets was S. avenae > M. dirhodum > R. padi. All aphid‐fruit fly diets resulted in larger offspring than a diet of only D. melanogaster, with the overall largest offspring being produced on the diet of M. dirhodum and fruit flies.     

Prey selection by linyphiid spiders: molecular tracking of the effects of alternative prey on rates of aphid consumption in the field

A molecular approach, using aphid-specific monoclonal antibodies, was used to test the hypothesis that alternative prey can affect predation on aphids by linyphiid spiders. These spiders locate their webs in cereal crops within microsites where prey density is high. Previous work demonstrated that of two subfamilies of Linyphiidae, one, the Linyphiinae, is web-dependent and makes its webs at sites where they were more likely to intercept flying insects plus those (principally aphids) falling from the crop above. The other, the Erigoninae, is less web-dependent, making its webs at ground level at sites with higher densities of ground-living detritivores, especially Collembola. The guts of the spiders were analysed to detect aphid proteins using enzyme-linked immunosorbent assay (ELISA). Female spiders were consuming more aphid than males of both subfamilies and female Linyphiinae were, as predicted, eating more aphid than female Erigoninae. Rates of predation on aphids by Linyphiinae were related to aphid density and were not affected by the availability of alternative prey. However, predation by the Erigoninae on aphids was significantly affected by Collembola density. Itinerant Linyphiinae, caught away from their webs, contained the same concentration of aphid in their guts as web-owners. However, nonweb-owning Erigoninae, living away from Collembola aggregations at web-sites, contained significantly higher concentrations of aphid. For both subfamilies there was evidence of a disproportionate increase in predation on aphids once Collembola populations had declined. It was concluded that nonaphid prey, by helping to maintain spiders in the field, can significantly affect predation on aphids.     

Evaluation of lycosid,micryphantid and linyphiid spiders as predators ofRhopalosiphum padi (Hom.: Aphididae) and their functional response to prey density-laboratory experiments

Laboratory experiments were performed to determine the potential of dominant spider species in winter wheat in Germany,Erigone atra (Blackwall),Lepthyphantes tenuis (Blackwall) andPardosa agrestis (Westring) adults and youngs, in suppressing the population ofRhopalosiphum padi (L.) on wheat plants and their functional response to different aphid densities. The presence of spiders significantly caused between 34 and 58% reduction in aphid population development on wheat plants compared to the aphid population in the absence of spiders. The functional response curves for these spiders as predators ofR. padi seem to descrive a typical type II functional response with the prey consumed increasing to a plateau as aphid densities increased. Prey killed without eating was linear on prey density.     

The effect of landscape complexity and microclimate on the thermal tolerance of a pest insect

Landscape changes are known to exacerbate the impacts of climate change. As such, understanding the combined effect of climate and landscape on agroecosystems is vital if we are to maintain the function of agroecosystems. This study aimed to elucidate the effects of agricultural landscape complexity on the microclimate and thermal tolerance of an aphid pest to better understand how landscape and climate may interact to affect the thermal tolerance of pest species within the context of global climate change. Meteorological data were measured at the landscape level, and cereal aphids (Sitobion avenae, Metopolophium dirhodum and Rhopalosiphum padi) sampled, from contrasting landscapes (simple and complex) in winter 2013/2014 and spring 2014 in cereal fields of Brittany, France. Aphids were returned to the laboratory and the effect of landscape of origin on aphid cold tolerance (as determined by CT_min) was investigated. Results revealed that local landscape complexity significantly affected microclimate, with simple homogenous landscapes being on average warmer, but with greater temperature variation. Landscape complexity was shown to impact aphid cold tolerance, with aphids from complex landscapes being more cold tolerant than those from simple landscapes in both winter and spring, but with differences among species. This study highlights that future changes to land use could have implications for the thermal tolerance and adaptability of insects. Furthermore, not all insect species respond in a similar way to microhabitat and microclimate, which could disrupt important predator–prey relationships and the ecosystem service they provide.     

A 3-year field-scale monitoring of foliage-dwelling spiders (Araneae) in transgenic Bt maize fields and adjacent field margins

Concerns have been raised that genetically modified Bt maize may harm non-target organisms, and there is a general call and need for a risk assessment of Bt maize. Spiders are important pest predators in agroecosystems and in maize, and can be exposed to the Bt toxin by herbivorous or pollen-collecting prey, by active Bt maize pollen feeding, and by ingesting their pollen-dusted webs. The foliage-dwelling spider fauna of Bt maize fields and adjacent margins was monitored and compared to non-transgenic maize fields. The study took place during the vegetation seasons of 2001–2003 in Bavaria, South Germany. Maize fields and adjacent nettle field margins were colonized by a typical spider assemblage, dominated by space-web spiders (Theridiidae and Linyphiidae). Abundance and species richness of spiders was higher in nettle margins than in maize fields. The proportion of hunting spiders tended to be higher in nettle margins, whereas space-web spiders tended to be more frequent in maize fields. Bt maize showed no consistent effect on individual numbers, species richness and guild structure of spiders in maize fields and adjacent nettle field margin strips. The spider abundance was higher in Bt treatments in 2003, whereas in 2001 and 2002 no significant differences were found. The results provide an important contribution for the implementation of case-specific and general surveillance of transgenic plants to be employed due to the regulations of the European Community.     

Various competitive interactions explain niche separation in crop‐dwelling web spiders

Competition for resources is a major organizing principle in communities of organisms that share similar ecological niches. Niche separation by means of exploitation or interference competition was investigated in two taxa of crop‐inhabiting spiders that overlap in microhabitat use and have similar web design. Competition for prey and web sites was tested in microcosm experiments with the most common species that build sheet‐webs: Enoplognatha gemina (Theridiidae) and Alioranus pastoralis (Linyphiidae). A field survey over the crop season provided data on spatial and temporal dispersion of Enoplognatha spp. (Theridiidae) and linyphiid spiders (Linyphiidae) and on availability of prey over the season. In the microcosm experiments, both taxa took springtails as prey, but only Enoplognatha fed on aphids. Differences in diet, however, could not be attributed to either exploitative or interference competition. Spatial separation of websites was attained by vertical displacement of webs in the vegetation (Enoplognatha) and by avoidance of patches occupied by conspecific or heterospecific individuals (linyphiids). In the field, densities of linyphiids and Enoplognatha were correlated negatively and webs were over‐dispersed relative to a random distribution. Both taxa colonized the field at the start of the season; linyphiids colonized as adults, quickly reproduced, and had a second adult peak; Enoplognatha matured in the middle of the season and their numbers remained fairly constant over the season. The combined experimental manipulations and field data suggest that niche separation occurs at different scales. The hypothesis of competition for websites was partially supported, while prey preference (or tolerance) and temporal differences in life history stages also may explain the negative correlations between densities of the two taxa.     

Food quality of Ephestia eggs,the aphid Rhopalosiphum padi and mixed diet for Orius majusculus

We studied the food quality of the aphid Rhopalosiphum padi to the pirate bug Orius majusculus using Ephestia eggs as high-quality comparison prey. Several performance parameters were tested on individuals that had been reared and maintained on each of the two single-prey diets or on a mixed diet. All fitness parameters were lower in individuals fed aphids only, indicating poor food quality of this prey. Compared with the pure Ephestia egg diet, the mixed diet enhanced teneral mass, while adult survival and female starvation tolerance were negatively affected and all other traits were unaffected. Body protein proportions were constant across diets, whereas lipid proportion was low in the aphid treatment. Preference for aphids was lower following a monotypic aphid diet than when reared on Ephestia eggs or a mixed diet. The results confirm that R. padi is low-quality food for O. majusculus as it is for other generalist predators, even though O. majusculus may contribute significantly to population suppression of the aphid.     

Management intensity and vegetation complexity affect web-building spiders and their prey

Agricultural management and vegetation complexity affect arthropod diversity and may alter trophic interactions between predators and their prey. Web-building spiders are abundant generalist predators and important natural enemies of pests. We analyzed how management intensity (tillage, cutting of the vegetation, grazing by cattle, and synthetic and organic inputs) and vegetation complexity (plant species richness, vegetation height, coverage, and density) affect rarefied richness and composition of web-building spiders and their prey with respect to prey availability and aphid predation in 12 habitats, ranging from an uncut fallow to a conventionally managed maize field. Spiders and prey from webs were collected manually and the potential prey were quantified using sticky traps. The species richness of web-building spiders and the order richness of prey increased with plant diversity and vegetation coverage. Prey order richness was lower at tilled compared to no-till sites. Hemipterans (primarily aphids) were overrepresented, while dipterans, hymenopterans, and thysanopterans were underrepresented in webs compared to sticky traps. The per spider capture efficiency for aphids was higher at tilled than at no-till sites and decreased with vegetation complexity. After accounting for local densities, 1.8 times more aphids were captured at uncut compared to cut sites. Our results emphasize the functional role of web-building spiders in aphid predation, but suggest negative effects of cutting or harvesting. We conclude that reduced management intensity and increased vegetation complexity help to conserve local invertebrate diversity, and that web-building spiders at sites under low management intensity (e.g., semi-natural habitats) contribute to aphid suppression at the landscape scale.     

Perception of olfactory aposematic signals by jumping spiders

Studies of aposematism are mostly focused on visual aspects of warning signalization and based on experiments with avian predators. This study presents results of experiments with an arthropod predator, a jumping spider Evarcha arcuata (Araneae: Salticidae) and olfactory (i.e., noncontact chemical) aposematic signals. Spiders were presented with chemically protected firebug Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). After acquiring the negative experience with the bugs, the spiders were offered a choice between the firebug olfactory signal and a scentless control. Spiders actively avoided the firebug signal, showing that they are able to recognize an unprofitable prey by means of olfactory chemoreception. The results show that olfactory signals alone may function as effective means of aposematic signalization to spiders.     

Identification of trophic interactions between <Emphasis Type="Italic">Macrolophus caliginosus</Emphasis> (Heteroptera: Miridae) and <Emphasis Type="Italic">Myzus persicae</Emphasis> (Homoptera: Aphididae) using real time PCR

Understanding food web interactions in native or agricultural ecosystems is an important step towards establishing sustainable pest management strategies. While the role of generalist predators as biological control agents is increasingly appreciated, the study of trophic interactions between individual predator species and their prey provides practical difficulties. Recently, different approaches have been suggested to determine prey items from predator guts using molecular methods. Macrolophus caliginosus is a generalist predator active in herbaceous agro-ecosystems. We developed a system to identify the DNA of its prey after ingestion, using Myzus persicae as a model. Esterase (MpEST) and cytochrome oxidase I (MpCOI) genes were targeted in the aphid, while M. caliginosus COI gene was used as control for predator DNA. Real time PCR proved to be specific and sensitive enough to detect prey DNA upon ingestion after feeding experiments. The system provided a linear amplification response with only 10 fg of prey genomic DNA as template. The detection system of MpCOI gene was more sensitive than MpEST, while the detection period was similar for both genes. Possibilities for using the system in ecological and biosafety studies with regard to sustainable pest management are discussed.

Invertebrate biodiversity affects predator fitness and hence potential to control pests in crops

Natural enemies that control pests usually allow farmers to avoid, or reduce, the use of pesticides. However, modern farming practices, that maximize yields, are resulting in loss of biodiversity, particularly prey diversity. Does this matter? Pests continue to thrive, and without alternative prey the predators should, perforce, concentrate their attentions upon the pests.We showed that a diverse diet significantly enhances predator fecundity and survival. Experiments were conducted using common generalist predators found in arable fields in Europe, the carabid beetle Pterostichus melanarius (Coleoptera: Carabidae) and the linyphiid spider Erigone atra (Araneae: Linyphiidae). We tested the hypothesis that mixed species diets were optimal, compared with restricted diets, with respect to parameters such as predator weights, egg weights, numbers of eggs laid, egg development times, egg hatching rates and predator survival. In carabids, an exclusive earthworm diet was as good as mixed diets containing earthworms for egg production and hatching, but less good than such mixed diets for increase in beetle mass and sustained egg laying. For spiders, aphids alone (Sitobion avenae) or with the Collembola Folsomia candida, drastically reduced survival. Aphids plus the Collembola Isotoma anglicana improved survival but only aphids with a mixed Collembola diet maximized numbers of hatching eggs.Predators offered only pests (slugs or aphids) had lowest growth rates and fecundity. We therefore demonstrated that conservation of a diversity of prey species within farmland, allowing predators to exploit a diverse diet, is essential if predators are to continue to thrive in crops and regulate agricultural pests.     

Foraging advantages of mixed-species association between solitary and colonial orb-weaving spiders

This study investigated association between solitary orb-weaving spiders and a colonial orb-weaving spider, Metepeira incrassata (Araneae: Araneidae). Spiders were sampled along transects and an index of species association showed that two of the species were associated more frequently than expected based on a null hipothesis of random co-occurrence. The potential advantages of mixed-species association were investigated by comparing prey-capture success of one of these associates, Nephila clavipes (Araneae: Tetragnathidae), when it occurs alone, in single-species groups, and when associated with M. incrassata colonies. Field observations of prey-capture success by all three of these categories of N. clavipes revealed that individuals in M. incrassata colonies captured significantly more prey than solitaries or individuals in single-species groups. The increase in prey capture by N. clavipes in M. incrassata colonies may result from utilization of a foraging niche which intercepts a diffirent spectrum of prey than that available to single-species groups or solitaries. Related to this enhanced prey consumption is greater fecundity of spiders in association with M. incrassata as compared to solitaries or individuals in single-species groups.     

Pollen interception by linyphiid spiders in a corn agroecosystem: implications for dietary diversification and risk-assessment

Dietary diversification, including consumption of plant tissues such as pollen, can enhance the fecundity of generalist predators, resulting in improved control of pest prey. Supplemental pollen feeding has been observed in many natural enemies, including sheet-web spiders (Araneae: Linyphiidae), which represent a major component of food webs in agroecosystems. Their horizontal, ground-based webs have the potential to intercept pollen grains during anthesis of crop plants, providing the opportunity for consumption of pollen to occur. In laboratory feeding trials, Frontinella communis and Tennesseellum formicum (Araneae: Linyphiidae) readily fed on pollen grains dusted on their webs, with 82 and 92% of spiders consuming pollen within the 210 min trial. These results revealed a strong potential for dietary supplementation with pollen in ground-based sheet-web spiders, indicating that pollen feeding may be an important component of the feeding biology of linyphiids. To measure pollen and prey interception in simulated linyphiid webs, a 20 m × 20 m grid of miniature sticky traps was established within and downwind of a corn agroecosystem. Traps were exposed for 24 h, all intercepted material was transferred to the laboratory for subsequent identification, and replaced with additional traps for 28 consecutive days in July and August 2008, to encompass periods before, during and after anthesis. Over 150,000 corn pollen grains and 5,000 prey items (dominated by Collembola and Hemiptera) were intercepted at simulated web-sites. Dates of peak anthesis resulted in pollen counts as high as 4,000 grains per web-site in the interior of the cornfield. Spatial Analysis by Distance Indices (SADIE) indicated significant temporal and spatial variability in pollen interception within and outside the corn field, but interestingly there was no significant spatial association between pollen and prey. Furthermore, transgenic Bacillus thuringiensis corn expresses insecticidal proteins in pollen, posing an exposure risk to non-target arthropods. Consumption of corn pollen may be a route to transgenic protein exposure in this important taxon of generalist predators.     

The impact of spiders and high temperatures on cereal aphid (Rhopalosiphum padi) numbers in an irrigated perennial grass pasture in South Australia

Spiders were the most important group of aphid natural enemies in an irrigated perennial grass pasture. The Lycosidae and Linyphiidae were the only families encountered. An exclusion experiment found predation by spiders to be an important factor in controlling aphid numbers. Together with high temperatures, they maintained aphid numbers at a lower than expected level.