Behavioural modification of a social spider by a parasitoid wasp

1. Manipulation of host behaviour by parasitoids has long captured the imagination of ecologists. Parasitoid wasps in the Polysphincta group of genera develop as external parasitoids of spiders. 2. In the present study, the previously undescribed interaction between a Zatypota sp. wasp (Ichneumonidae) and a social spider Anelosimus eximius (Theridiidae) is described. The larva of this Zatypota wasp is found to induce its host to disperse from their communal web and build an entirely enclosed web consisting of densely spun silk. 3. The wasp is observed to target primarily immature A. eximius individuals, with 37.5–44% of nests in a given area being parasitised. Of those nests, approximately 1.3–2.0% of individuals are hosts to the parasitoid larvae. Larger spider colonies had a significantly higher probability of harbouring parasitoids. 4. This interaction results in unusual behaviours for A. eximius induced by the parasitoid: (i) leaving the protection of the social nest and (ii) building a unique, altered web that it would not otherwise build. It is suggested that the wasp may be tapping into ancestral dispersal behaviours in its host and that a social species provides this wasp an evolutionary advantage by allowing a stable host source.     

The parasitoid wasp Eruga unilabiana Pádua & Sobczak,sp. nov. (Hymenoptera: Ichneumonidae) induces behavioral modification in its spider host

Some polysphinctine parasitoid wasps can alter the web building behavior of their host spiders. In this paper, we describe and illustrate a new species Eruga unilabiana sp. nov. and report for the first time, to the best of our knowledge, the interaction between this parasitic wasp and the linyphiid spider Dubiaranea sp. We investigated the wasp's host selection, development, and manipulation of host behavior. We found that most of the parasitized spiders were intermediate‐sized adult females that probably provide sufficient resources for parasitoid larvae and are less vulnerable for parasitoid females than larger host individuals at attack. The cocoon web of Dubiaranea sp. consists of a complex three‐dimensional tangle structure with several non‐stick radial lines that converge at the cocoon. In addition, E. unilabiana individuals construct their cocoons horizontally, which differ from cocoons of the majority of polysphinctine wasps. This study provides important information and discussion to further understand the evolution of parasitoid wasp–spider interactions.     

Wasp Attacks and Spider Defence in the Orb Weaving Species <Emphasis Type="Italic">Zygiella x-notata</Emphasis>

Predator–prey relationships are generally based on arm-race. Wasps and spiders are both predators, which could be potential prey for each other. The orb weaver spider Zygiella x-notata is sometimes a prey for the wasp Vespula germanica. We observed the wasp hunting behaviour under natural conditions, and we tested the influence of the spider’s behaviour on the wasp attack success. Wasps were active predators during the reproductive period of the spider. Results showed that wasps located more easily male spiders than females particularly when they were engaged in mate guarding. Female location depended on the presence of a web, but also of prey or prey remains in the web. On the other hand, their location depend neither on the characteristics and the position of the retreat in the environment nor on the size of the web. After location, males were more often captured than females whatever their behaviour (mate guarding or not). Presence of prey remains or prey in the web did not increase the risk for the spider to be captured. There was also no influence of the retreat’s characteristics or of its position in the habitat on the risk for the spider to be captured; but wasp successful attacks were less numerous when silk was present around the entrance of the retreat or when the spider was completely inside. As prey and prey remains favoured location of spiders by the wasps, we tested spider web cleaning behaviour as a response to wasp predatory pressure. By throwing small polystyrene pellets in the webs, we observed that more 80% of the spiders rejected the pellets in less than one minute. Our data indicated that wasps were significant predators of Z. x-notata and wasp attack could have been a selective pressure that had favoured spider defensive behaviours such as web cleaning.     

Tool Use by Spiders: Stone Selection and Placement by Corolla Spiders Ariadna (Segestriidae) of the Namib Desert

The corolla spider (Araneae: Segestriidae: Ariadna) of the Namib Desert gravel plains typically places seven or eight stones in a circle around its burrow entrance. It was examined whether the spider selects and places stones according to physical characteristics. Circle composition can be explained by the allometric scaling to spider size of the burrow entrance and the stones. The stones were usually placed with the narrowest side or point towards the burrow. Quartz crystals were preferred to four other stone types available. The spiders could detect prey brushing the outside of the circle stones that were about as wide as the spider's path of attack. I conclude that corolla spiders use the selected stones as tools to extend their foraging range.     

Testing adaptive significance of host manipulation with a parasitoid wasp

According to the extended phenotype hypothesis, certain parasites manipulate the host's behaviour which ultimately enhances the transmission of parasite genes into the next generation. The parasitoid wasp Ampulex compressa attacks and stings its cockroach Periplaneta americana host and lays an egg on the cockroach's leg. Before the wasp's oviposition, the stung cockroach engages in excessive self-grooming for about 30 min. The prey location hypothesis posits that self-grooming may allow the wasp to easily locate its host before transporting it to the nest. To test this hypothesis, we manipulated the mobility of the stung cockroach under different spatial constraints. Latencies to locate stung cockroaches with unlimited movement were similar than latencies to locate stung, but motionless cockroaches irrespectively of spatial constraints. Wasps were less willing to lay eggs and seal an entrance to the burrow in treatments with motionless cockroaches which suggests that if the expected reproductive success is low, then parental investment decreases. Our results provide no support for the location hypothesis and call for further experimental investigation of the extended phenotype hypothesis in parasite–host interactions.     

Resource Management in the Orb-Weaving Spider Zygiella x-notata: I. Influence of Spider Behaviour and Available Prey

Management of resource exploitation by the orb-weaving spider Zygiella x-notata was investigated in relation to available prey. Prey capture is studied according to prey type (cricket or fly), and the spider's behaviour (waiting without prey or consuming other prey), at the moment when a prey item was placed onto the web. Characteristics of the spider's exploitation of the previous item (feeding time, and quantities ingested) were analysed according to the type and quantity of prey presented, (1 or 2 items at 1-h intervals). Capture time did not vary in relation to prey type, nor spider activity. However, duration and quantities of certain behavioural components (biting and wrapping) did vary according to prey type and the spider's behaviour, at the moment of presentation of prey. Whatever the type of prey received, if the first item consumed was a cricket, the spiders reduced time spent feeding on this prey without any decrease in the quantities ingested.     

Prey Luring Coloration of A Nocturnal Semi‐Aquatic Predator

Body coloration serves a variety of purposes in animals. Diurnal and nocturnal predators such as spiders may use their body coloration to lure prey. We predicted here that the white patches on the forelegs on females of the nocturnal semi‐aquatic spider Dolomedes raptor lure prey, explaining why they are primarily displayed when the spider forages along the water edge. To test our prediction, we developed a color vision model assessing whether the patches are visible to pygmy grasshoppers, the spider's primary prey. We conducted a field experiment using cardboard dummies that resemble D. raptor in size, shape, and color, but with half of them lacking leg patches, and we staged interactions between pygmy grasshoppers and D. raptor with and without leg patches in a greenhouse. We found the white patches to be visible to grasshoppers. The dummies with white patches attracted more grasshopper prey than the dummies without the patches. Moreover, grasshoppers were more attracted to spiders when their white patches were present. Our results supported the hypothesis that the white patches of D. raptor lure prey. Our findings, nevertheless, could not be explained as the spider's body coloration acting as a sensory trap but it should not be ruled out. More studies on a wider range of predators and prey will give more meaningful insights into the co‐evolution of predatory lures and prey sensory modalities.     

Spider silk felting—functional morphology of the ovipositor tip of Clistopyga sp. (Ichneumonidae) reveals a novel use of the hymenopteran ovipositor

Apical serrations of the hymenopteran ovipositor have been widely postulated to originally constitute adaptations for cutting through hard substrates. Simplifications of the ovipositor tip have occurred in several ichneumonid wasp genera associated with spiders. Despite such reduction in Clistopyga (Hymenoptera, Ichneumonidae), the ovipositor still possesses some apical serrations. Through the first detailed study, we believe, on the behaviour of an ovipositing Clistopyga species, we show that it can alter its ovipositor for different purposes and that the primary function of the apical serrations is clinging to its spider host as the spider attempts to escape. Intriguingly, we also discover a hitherto undocumented adaptation for the hymenopteran ovipositor. The female wasp seals openings in the silken spider nest by using its ovipositor on the silk in a highly sophisticated way that is comparable to how humans entangle wool by needle felting. By studying the ovipositor morphology through a scanning electron microscope, we elucidate how this works, and we hypothesize that by closing the nest the female wasp protects its developing kin.     

Emergent properties in the behaviour of a virtual spider robot

Using a virtual spider robot, we studied hypotheses about the weaving behaviour of orb spiders. Our model spiders built virtual webs that mimicked perfectly the visual architecture of real webs of the garden cross spider Araneus diadematus. The matching of capture spiral and auxiliary spiral pitch was an apparently emergent property in both types of web. This validated our interpretation of the garden spider''s web-building decision rules, which use strictly local interactions with previously placed threads to generate global architecture.     

Complementary effects of resident natural enemies on the suppression of the introduced moth Epiphyas postvittana

Generalist predators may disrupt or complement biological control by parasitoids. Past studies have examined how predators and parasitoids interact to affect aphid suppression, but more information is needed from other host taxa. Here, we explore the interactive effects of a spider (Cheiracanthium mildei) and a generalist parasitoid (Meteorus ictericus) on the light brown apple moth (Epiphyas postvittana), a recent introduction to North America. The spider negatively affected adult parasitoids in a field experiment, and reduced numbers of parasitized larvae in the laboratory. Nonetheless, the combined effects of parasitoids and spiders on larval mortality of the moth were additive. Percent parasitism was not affected by the presence of the spider in field or laboratory experiments, and results were similar when single or multiple larval instars of the moth were included. The spider’s lack of prey preference for unparasitized or parasitized larvae likely precluded any disruptive effects on parasitism. Results suggest that resident generalist parasitoids and predators can work in conjunction to hinder the invasion success of a novel herbivore prey species.     

Parasitoid genus‐specific manipulation of orb‐web host spiders (Araneae,Araneidae)

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The effect of colour variation in predators on the behaviour of pollinators: Australian crab spiders and native bees

1. Australian crab spiders exploit the plant–pollinator mutualism by reflecting UV light that attracts pollinators to the flowers where they sit. However, spider UV reflection seems to vary broadly within and between individuals and species, and we are still lacking any comparative studies of prey and/or predator behaviour towards spider colour variation. 2. Here we looked at the natural variation in the coloration of two species of Australian crab spiders, Thomisus spectabilis and Diaea evanida, collected from the field. Furthermore, we examined how two species of native bees responded to variation in colour contrast generated by spiders sitting in flowers compared with vacant flowers. We used data from a bee choice experiment with D. evanida spiders and Trigona carbonaria bees and also published data on T. spectabilis spiders and Austroplebeia australis bees. 3. In the field both spider species were always achromatically (from a distance) undetectable but chromatically (at closer range) detectable for bees. Experimentally, we showed species‐specific differences in bee behaviour towards particular spider colour variation: T. carbonaria bees did not show any preference for any colour contrasts generated by D. evanida spiders but A. australis bees were more likely to reject flowers with more contrasting T. spectabilis spiders. 4. Our study suggests that some of the spider colour variation that we encounter in the field may be partly explained by the spider's ability to adjust the reflectance properties of its colour relative to the behaviour of the species of prey available.     

Are you what you eat? A highly transient and prey‐influenced gut microbiome in the grey house spider Badumna longinqua

Stable core microbial communities have been described in numerous animal species and are commonly associated with fitness benefits for their hosts. Recent research, however, highlights examples of species whose microbiota are transient and environmentally derived. Here, we test the effect of diet on gut microbial community assembly in the spider Badumna longinqua. Using 16S rRNA gene amplicon sequencing combined with quantitative PCR, we analyzed diversity and abundance of the spider's gut microbes, and simultaneously characterized its prey communities using nuclear rRNA markers. We found a clear correlation between community similarity of the spider's insect prey and gut microbial DNA, suggesting that microbiome assembly is primarily diet‐driven. This assumption is supported by a feeding experiment, in which two types of prey—crickets and fruit flies—both substantially altered microbial diversity and community similarity between spiders, but did so in different ways. After cricket consumption, numerous cricket‐derived microbes appeared in the spider's gut, resulting in a rapid homogenization of microbial communities among spiders. In contrast, few prey‐associated bacteria were detected after consumption of fruit flies; instead, the microbial community was remodelled by environmentally sourced microbes, or abundance shifts of rare taxa in the spider's gut. The reshaping of the microbiota by both prey taxa mimicked a stable core microbiome in the spiders for several weeks post feeding. Our results suggest that the spider's gut microbiome undergoes pronounced temporal fluctuations, that its assembly is dictated by the consumed prey, and that different prey taxa may remodel the microbiota in drastically different ways.     

Ineffective crypsis in a crab spider: a prey community perspective

Cryptic coloration is assumed to be beneficial to predators because of an increased encounter rate with unwary prey. This hypothesis is, however, very rarely, if ever, studied in the field. The aim of this study was to quantify the encounter rate and capture success of an ambush predator, in the field, as a function of its level of colour-matching with the background. We used the crab spider Misumena vatia, which varies its body colour and can thereby match the colour of the flower it hunts upon. We carried out a manipulative field experiment using a complete factorial design resulting in six different colour combinations of crab spiders and flowers differing in their degree of colour-matching. A rich and diverse set of naturally occurring insects visited the flowers while we continuously video-recorded the spider''s foraging activity. This enabled us to test the crypsis, the spider avoidance and the flower visitor attraction hypotheses, all three supported by previous studies. Flower visitors of different groups either avoided crab spiders independent of colour-matching, such as solitary bees and syrphid flies, or ignored them, such as bumble-bees and honeybees. Moreover, colour-matched spiders did not have a higher encounter rate and capture success compared to the visually apparent ones. Thus, our results support the spider avoidance hypothesis, reject the two other hypotheses and uncovered a fourth behaviour: indifference to predators. Because flower visitors reacted differently, a community approach is mandatory in order to understand the function of background colour-matching in generalist predators. We discuss our results in relation to the size and sociality of the prey and in relation to the functional significance of colour change in this predator.     

SIGNAL POLYMORPHISM IN THE WEB-DECORATING SPIDER ARGIOPE ARGENTATA IS CORRELATED WITH REDUCED SURVIVORSHIP AND THE PRESENCE OF STINGLESS BEES, ITS PRIMARY PREY

Abstract.— Many spiders, and in particular those in the genus Argiope, spin highly visible web decorations whose function and significance are the subject of spirited debate. In this work, we present data to address two of the competing hypotheses that fuel this controversy. In particular, we examine the relationship between the presence of web decorations and spider survivorship (predator‐protection hypothesis) and the relationship between the presence of prey and spider decorating behavior (the prey‐attraction hypothesis). Our laboratory studies reveal that the decorating behavior of the spider A. argentata has a genetic component but that the expression of decorating behavior tends to be elicited only when a spider is well fed. Furthermore, our field studies show that in the presence of abundant stingless bees, spider decorating behavior is induced. Nevertheless, our field surveys also suggest that spiders that decorate their webs show reduced survivorship. We propose that the high correlation between web decorating in the presence of stingless bees supports the hypothesis that A. argentata engage in decorating behavior when attracting or targeting specific prey types. However, we also propose that web decorations attract the predators of A. argentata because high‐frequency decorators suffer lower survivorship than spiders that decorate moderately or rarely. These findings suggest that spider web decorating behavior is affected by conflicting selection pressures: the positive effect of prey attraction versus the negative effect of predator attraction. Due to the heritable component of decorating behavior, web decorating among A. argentata is likely to be particularly sensitive to the spider's local ecology as well as local patterns of gene flow.     

“Veils” Against Predators: Modified Web Structure of a Host Spider Induced by an Ichneumonid Parasitoid, Brachyzapus nikkoensis (Uchida) (Hymenoptera)

When the larva of Brachyzapus nikkoensis, a koinobiont ectoparasitoid of Agelena limbata forming a funnel web, is a penultimate instar, “veils” of very fine and dense threads covering the spider and parasitoid larva were observed in the tunnel of funnel web. As the veils are not formed until the parasitoid became penultimate instar and the parasitoid larvae are on active hosts at this stage, the veils are considered to be formed by the spider under the manipulation of the parasitoid larva. Removal of the veil indicated that penultimate larvae and pupae were more likely to fail to emerge in manipulated webs compared to the controls. The modified web seems resistant against predators and scavengers such as ants. This is the first record of web modification demonstrating its resistance to predators.     

Trunk structural traits explain habitat use of a tree-dwelling spider (Selenopidae) in a tropical forest

Habitat selection by spiders may be strongly influenced by biotic, climatic, and physical factors. However, it has been shown that the selection of habitats by generalist predators (like spiders) is regulated more by the physical structure of the habitat than by prey availability. Yet, the preferences of spiders in relation to plants or plant traits remain poorly explored. In a remnant of the Atlantic forest in Brazil, the spider Selenops cocheleti is frequently detected on the trunks of plants from the Myrtaceae family. Here, we investigated quantitatively and experimentally whether the colonization of trees by S. cocheleti is related to plant species or the presence of specific structures on trunks. We found that S. cocheleti preferentially occurred on plants of the family Myrtaceae. This spider was also strongly associated with trees that have smooth trunks and/or exfoliating bark. Non-Myrtaceae plants that were occupied by this species have exfoliating bark (e.g., Piptadenia gonoacantha) or deep fissures on the trunk (e.g., the exotic species Pinus elliottii). Our results indicate that the selection of host plants by S. cocheleti is not species-specific, but based on the structural characteristics of plants. Trunks with exfoliating bark may benefit spiders by providing shelter against predators and harsh climatic conditions. Smooth surfaces might allow rapid movements, facilitating both attacks on preys and escape from predators. Our study emphasizes the importance of the physical structure of the habitat on spider's distribution. Future studies investigating how specific plant characteristics influence prey acquisition and predator avoidance would improve our understanding of habitat selection by these animals.     

Temporal asynchrony and spatial co-occurrence with the host: the foraging patterns of Nemka viduata, a parasitoid of digger wasps (Hymenoptera: Mutillidae and Crabronidae)

Studies which quantitatively analyse how aculeate parasitoids exploit their window of opportunity to find and attack a host are scarce, despite the recognized importance of parasitic pressure as a driving force that promotes aggregate nesting in their hosts. We have studied the activity and behaviour of the velvet ant Nemka viduata, an ectoparasitoid of immature stages of the digger wasp Stizus continuus. Due to the resource exploited by the parasitoid (mature larvae and prepupae), and in general agreement with basic optimal foraging theory, we expected a major activity at late stages of the host seasonal provisioning period, an independence from the host daily provisioning patterns and a spatial positive association with host nest density. In accordance with these predictions, during the season, the parasitoid resulted was more active at the end of the host provisioning period, and across the day, it showed an inverse quadratic pattern of activity, in contrast to the positive one shown by the host. Thus, at both temporal scales, N. viduata activity was highly asynchronous with that of the host. At a spatial scale, however, the activity of the velvet ants was correlated with host nest density, although there is weak evidence suggesting that areas of high host density suffered from a higher rate of parasitism. Multivariate analyses confirmed a number of relevant factors associated with velvet ants’ activity, including nest density (positive), air temperature and the hour of the day (both negative). In addition, the activity of both male S. continuus and male N. viduata entered in the models in association with female parasitoid’s activity, probably because of their mating strategy.     

Effect of abiotic factors on the foraging strategy of the orb‐web spider Argiope keyserlingi (Araneae: Araneidae)

Abstract Environmental conditions such as light level, background contrast and temperature might influence a spider's prey capture success and risk of predation. Thus it may often be advantageous for spiders to adjust web‐building behaviour in response to variation in these environmental conditions. This hypothesis was examined in a study of the construction of webs and web decorations (conspicuous strands of silk at the hub of the web) of the orb‐web spider Argiope keyserlingi. Web decorations are thought to have one or more separate functions. They may attract prey, deter predators or advertise the web to oncoming birds, thus preventing web damage. In this series of experiments, relationships between weather parameters and the construction of webs and web decorations were considered. In complementary laboratory experiments, A. keyserlingi spiders were exposed to two different light levels (700 and 90 lx), background contrasts (black and white) and temperature conditions (20 and 26°C). Of the available weather parameters, only temperature was significantly related to web decorating behaviour but not to web size. In the laboratory, temperature also influenced web‐decorating behaviour, and spiders in dim light (700 lx) constructed larger webs and longer decorations. Background contrast did not significantly alter web size or web decorations. These data suggest that when prey availability is reduced at low temperatures, spiders may use web decorations to attract prey to the web. Similarly, in dim light, spiders may build more and larger decorations to increase the visual signal to approaching prey or to advertise the web to oncoming birds.     

Attack Behavior of Two Wasp Species of the <Emphasis Type="Italic">Polysphincta</Emphasis> Genus Group (Hymenoptera,Ichneumonidae) on their Orb-Weaver Spider Hosts (Araneae,Araneidae)

Species in the Polysphincta genus group, as far as is known, are exclusively koinobiont ectoparasitoids of spiders. These wasps attack their hosts, inflicting a temporary paralysis, and then lay one egg on the host’s abdomen or prosoma. Parasitoid attack behavior is highly variable among species, including occasions where the wasp darts directly and holds the spider, as well as instances involving complex behavioral sequences. In the present study, we describe the attack behavior of Polysphincta sp. nr. purcelli and P. janzeni on Cyclosa fililineata and C. morretes, respectively. All attacks occurred at night. Initially, the female wasp landed on the web hub at the position occupied by the spider, with the spider always escaping from this initial attack. Subsequently, the wasp waited for up to 14 h at the web hub for the spider’s return. The wasp then inserted its ovipositor into the mouth of the spider, after which the spider became paralyzed and remained motionless for at least 30 min. The wasp laid one egg on the surface of the host’s abdomen and remained on the web for at least 1 h thereafter. The lie-in-wait and attack only after the return of the host to the web hub, as well as the permanence of the wasp on the web after the attack are not frequent behaviors described for polysphinctines. Behavioral idiosyncrasies, such as those observed here, are common among polysphinctines, suggesting a high level of specific adaptive matching of polysphinctine parasitoid behavior to their hosts’ biological characteristics.