Predator foraging behavior in response to perception and learning by its prey: interactions between orb-spinning spiders and stingless bees

Although rewarded bees learn and remember colors and patterns, they have difficulty in learning to avoid negative stimuli such as decorated spider webs spun by Argiope argentata. A. argentata decorates its web with silk patterns that vary unpredictably (Fig. 1) and thus foraging insects that return to sites where spiders are found encounter new visual cues daily. Stingless bees can learn to avoid spider webs but avoidance-learning is slowed or inhibited by daily variation in web decorations (Figs. 3,4; Tables 1,2). In addition, even if bees learn to avoid decorated webs found in one location, they are unable to generalize learned-avoidance responses to similarly decorated webs found at other sites. A. argentata seems to have evolved a foraging behavior that is tied to the ways insects perceive and process information about their environment. Because of the evolutionary importance of bee-flower interdependence, the predatory behavior of web-decorating spiders may be difficult for natural selection to act against.     

Signals for damage control: web decorations in <Emphasis Type="Italic">Argiope keyserlingi</Emphasis> (Araneae: Araneidae)

Orb web spiders of the genus Argiope are permanently located at the hub of the orb web and are thus vulnerable to changing environmental conditions. Severe damage to the web by non-prey animals can have a significant impact on survival, through the cost of producing expensive silk and the loss of foraging opportunities. Thus, selection should favor web protection mechanisms, and the conspicuous web decorations, typical of Argiope spiders, may play a role. Decorated webs suffer less damage than undecorated webs, consistent with the view that they advertise the presence of the web to non-prey animals that may damage the web. However, whether spiders respond to web damage by increasing investment in web decorations has not been investigated. We subjected adult St. Andrew's Cross spider (Argiope keyserlingi) females to three levels of web damage and recorded their subsequent web-decorating behavior. Mild damage, similar to that caused by impacting prey, did not affect either web building or decorating behavior. However, spiders subjected to substantial web damage both reduced the size of subsequent webs and increased investment in web decoration size. These data are consistent with an advertising role of web decorations.     

Why do nocturnal orb-web spiders (Araneidae) search for light?

The nocturnal orb-web spider Larinioides sclopetarius lives near water and frequently builds webs on bridges. In Vienna, Austria, this species is particularly abundant along the artificially lit handrails of a footbridge. Fewer individuals placed their webs on structurally identical but unlit handrails of the same footbridge. A census of the potential prey available to the spiders and the actual prey captured in the webs revealed that insect activity was significantly greater and consequently webs captured significantly more prey in the lit habitat compared to the unlit habitat. A laboratory experiment showed that adult female spiders actively choose artificially lit sites for web construction. Furthermore, this behaviour appears to be genetically predetermined rather than learned, as laboratory-reared individuals which had previously never foraged in artificial light exhibited the same preference. This orb-web spider seems to have evolved a foraging behaviour that exploits the attraction of insects to artificial lights. Received: 8 June 1998 / Received in revised form: 18 January 1999 / Accepted: 19 January 1999     

Parent-offspring aggression in moorhens

Summary Colonial orb-weaving spiders from Mexico were studied to test predictions of risksensitive foraging theory: 1. group foraging increases prey capture/individual, and reduces prey variance; 2. spiders should be expected to exhibit risk-averse behavior (forage in groups) when the average level of prey exceeds individual needs, and exhibit risk-prone behavior (forage solitarily) when prey are searce. Laboratory and field studies show that group foraging increases capture efficiency and reduces variability in prey captured per spider. In desert/mesquite grassland habitat, where prey availability is low, M. atascadero forage solitarily in most cases. In tropical rainforest/agriculture sites, M. increassata forage in large colonies of thousands of webs. In intermediate habitats, M. spinipes forages solitarily or in groups, depending on prey availability. Over a range of sites with varying levels of prey, M. spinipes shifts from a risk-prone to a risk-averse group foraging strategy as prey increases.Group foraging behavior observed in colonial Metepeira fits the predictions of risk-sensitive foraging models. These findings explain why spiders tend to group webs together only in areas of superabundant prey. The role of risk-sensitivity in the evolution of coloniality in spiders is discussed.     

A predator’s body coloration enhances its foraging profitability by day and night

Few predators forage by both day and night. It remains unknown, however, how the costs and benefits of foraging or signaling are partitioned in animals that forage at all times. The orb-web spider Cyrtophora moluccensis is brightly colored and forages by day and night. We determined the benefits reaped when it forages by both day and night by estimating the biomass of prey caught in their webs. Additionally, we quantified whether the spider’s presence influences the number of prey caught by day and night and whether its colorful body is visible to diurnal and/or nocturnal insects using diurnal and nocturnal insect vision models. We found that approximately five times the biomass of prey was caught in C. moluccensis’ webs by night than by day. Hemipterans, hymenopterans, and dipterans were predominantly caught by day, while lepidopterans (moths) were predominately caught by night. Accordingly, we concluded that foraging by night is more profitable than foraging by day. We predicted that other benefits, for example, energetic advantages or enhanced fecundity, may promote its daytime activity. Foraging success was greater by day and night when the spider was present in the web than when the spider was absent. We also found that parts of the spider’s body were conspicuous to diurnal and nocturnal insects, possibly through different visual channels. The colorful body of C. moluccensis, accordingly, appears to influence its foraging success by attracting prey during both the day and night.     

Trap barricading and decorating by a well-armored sit-and-wait predator: extra protection or prey attraction?

Animals may build multiple structures to provide benefits to counter the costs of building. Many orb web spiders add multiple structures, e.g., barricading barrier webs and silk decorations, to their webs and these structures have been hypothesized to function to deter predators or attract prey. The heavily armored spiny spiders construct barrier webs around their orb webs and decorate them with conspicuous silk tufts. Why these organisms, already well protected by a thick cuticle and spines, make the extra investment of building barrier webs and adding conspicuous silk decorations is not known. We predicted that these structures function to both attract prey and deter predators. Field experiments were conducted in two consecutive years using orb webs built by the East Asian spiny spider Thelacantha brevispina. We either (1) concealed the decoration, (2) removed the barrier webs, or (3) left the decorations and barrier webs intact. We found year and treatment to interactively influence prey interception rates. In 2010, but not in 2009, we found prey interception with T. brevispina webs to be greater when the decorations were conspicuous than when they were concealed suggesting that the decorations may lure prey. Prey interception was lower when the barrier webs were present without decorations compared to when they were absent without decorations. The prey-attracting function of the decorations thus may counter the reduction in prey interception incurred by adding a barrier web. Predatory wasp interactions were not influenced by any of our treatments, probably because the spiders’ thick cuticle is the primary means of protection from wasps. Bird predation events, while rare, occurred only when decorations were concealed or the barrier webs were removed. It is therefore plausible that the tuft decorations both lure prey and deter birds.     

Defensive behavior of the black widow spider Latrodectus hesperus (Araneae: Theridiidae)

Summary When threatened, the black widow spider, Latrodectus hesperus, emits an adhesive, viscous web, pulls the strand from its spinnerets with its fourth pair of legs, and spreads its appendages. This behavior positions the web over the delicate abdomen, increases the area of protection, and enables the spider to place the web onto the offender, if necessary.In laboratory interactions, the viscous web protected black widows from mice (Peromyscus spp.). Mature female spiders, which had their spinnerets blocked and hence could not discharge the viscid silk, escaped less often than did black widows that were not experimentally altered.The viscid silk is palatable to mice and it appears that the deterrent effect of the web is due solely to mechanical irritation.The defensive behavior is elicited most often from mature females, which may suffer greater predation than other age groups. Males lose the ability to produce the defensive web at maturity and may shift their energy resources totally into reproductive effort.     

Do social spiders cooperate in predator defense and foraging without a web?

Nearly all social spiders spin prey-capture webs, and many of the benefits proposed for sociality in spiders, such as cooperative prey capture and reduced silk costs, appear to depend on a mutually shared web. The social huntsman spider, Delena cancerides (Sparassidae), forms colonies under bark with no capture web, yet these spiders remain in tightly associated, long-lasting groups. To investigate how the absence of the web may or may not constrain social evolution in spiders, we observed D. cancerides colonies in the field and laboratory for possible cooperative defense and foraging benefits. We observed spiders’ responses to three types of potential predators and to prey that were introduced into retreats. We recorded all natural prey capture over 447 h both inside and outside the retreats of field colonies. The colony’s sole adult female was the primary defender of the colony and captured most prey introduced into the retreat. She shared prey with younger juveniles about half the time but never with older subadults. Spiders of all ages individually captured and consumed the vast majority of prey outside the retreat. Young spiders benefited directly from maternal defense and prey sharing in the retreat. However, active cooperation was rare, and older spiders gained no foraging benefit by remaining in their natal colony. D. cancerides does not share many of the benefits of group living described in other web-building social spiders. We discuss other reasons why this species has evolved group living.     

Material investment and prey capture potential of reduced spider webs

Summary The webs of Miagrammopes animotus have a simple structure and variable form. However, both the length of their lines and the total surface area of their capture threads are closely associated with spider size. These spiders' ability to deposit both linear and looped cribellar capture threads along a web's diverging capture lines plays an important role in establishing these relationships. Looped capture threads have the greater surface area and are more prominent in the webs of older spiders where they increase a web's surface area and enhance its ability to retain prey. The predicted performance of these webs is supported by comparisons of the stickiness of their threads and a survey of the prey their owners capture. Cribellar thread stickiness increases with spider size, and larger spiders capture prey that have greater masses.     

Three-dimensional barricading of a predatory trap reduces predation and enhances prey capture

Animal structures come at material, energetic, time, and expression costs. Some orb-web spiders add three-dimensional barrier structures to their webs, but many do not. Predator protection is considered to be the principal benefit of adding these structures. Accordingly, it remains paradoxical why some orb-web spiders might construct the barriers while others do not. Here, we experimentally determined whether the barrier structure added to the horizontal orb web of the spider Cyrtophora moluccensis deters predators at the cost of reducing the amount of prey captured in the field. We conducted experiments by day and night to assess whether the effects vary with the time of day. We found that the three-dimensional barriers not only offered protection from predatory wasps by day but also enhanced the amount of prey captured by day and night. Moreover, the barrier structure appears particularly useful at catching moths, the largest and most energetically profitable prey that it encounters. We, therefore, concluded that reducing the energetic and time costs associated with producing and depositing extra silk threads is the principal reason why barrier structures are used intermittently among orb-web spiders.     

Cooperative web sharing against predators promotes group living in spider mites

I examined spider mite cooperative web sharing against predation as a factor promoting group living. Tetranychus urticae and Tetranychus kanzawai infest leaf surfaces under webs made of silk threads. Experimental observation of predation by the predatory mite Euseius sojaensis on spider mites of different group sizes revealed that fewer spider mites were preyed upon when the web-building period before the attack was prolonged, suggesting that established webs help protect spider mites. Moreover, per capita predation on spider mites was diluted in larger groups. This was not due to predator satiation but seemingly because webs had been completed while the initial prey was consumed. Spider mites lived more closely together in the presence of a predator, showing that the degree of group living is facultative. In the presence of a preceding spider mite with an established web, a newcomer spider mite gain protection by taking residence in the established webs; sharing the web was not disadvantageous for the preceding mite. The proportion of individuals preyed upon did not differ between preceding and newcomer mites, suggesting that there was no interference against the latter. These interactions were consistent between heterospecific spider mites. Because there was no detectable indirect interaction between mites sharing fresh webs, cooperative web sharing seemed to be a major force promoting group living in the spider mites. Moreover, the distances between spider mites did not differ between heterospecific and conspecific groups, demonstrating that mites living together do not distinguish between species; hence, heterospecific mites may cooperate and live together in the same manner as conspecifics.     

Social spider defense against kleptoparasitism

Summary Because of the large amount of webbing they provide, social spider colonies often host other satellite spider species referred to as kleptoparasites or food stealers. Such kleptoparasites may take advantage of increased prey capture rates associated with large spider aggregations. This study investigated the relationship between a cooperatively social spider species, Anelosimus eximius (Araneae: Theridiidae), which lives in the undergrowth of tropical rainforests in Peru, and its kleptoparasite, Argyrodes ululans (Araneae: Theridiidae), which specializes in foraging in An. eximius webs. Although large aggregates of spiders may be more attractive to kleptoparasites, the benefits of group defense may offset this cost. Natural colonies were observed, and enclosed field colonies containing fixed numbers of host spiders were manipulated in order to determine whether kleptoparasite success is affected by the number of social spiders that are available for defense. Prey was less likely to be stolen by Ar. ululans when a greater number of host An. eximius spiders were involved in prey capture. When hosts detected a kleptoparasite earlier and chased it more often, prey was more likely to be successfully defended. Ar. ululans was more successful in stealing small prey items in all colonies and gave up more readily on very large prey (> 11 mm). I conclude that communal living and group defense in An. eximius confer protection from the kleptoparasite Ar. ululans.     

Functional values of stabilimenta in a wasp spider, Argiope bruennichi: support for the prey-attraction hypothesis

Many orb-weaving spiders decorate their webs with conspicuous ultraviolet (UV)-reflective stabilimenta. The prey-attraction hypothesis suggests that stabilimenta are visually attractive to prey and thus may increase the spiders’ foraging success. However, previous studies on the function of stabilimenta have produced conflicting results in Argiope species. Using a combination of field and laboratory studies, we examined whether the linear stabilimentum of Argiope bruennichi contributes to prey interception. We recorded prey interceptions in 53 webs with stabilimenta and 37 equally-sized webs without stabilimenta, classifying captured prey according to their taxonomical group and size. On average, 6.2?±?4.7 prey items were intercepted in webs with stabilimenta, while 3.2?±?2.9 items were intercepted in webs without stabilimenta. The effects of stabilimenta on foraging success appear to be due to increased interception of UV-sensitive insect pollinators, including 20 families of Diptera, Hymenoptera, Coleoptera, and Lepidoptera. The mean number of UV-sensitive prey was 4.4?±?3.6 in webs with stabilimenta compared with 1.8?±?2.1 in webs without stabilimenta. Webs with and without stabilimenta did not differ in the mean number of UV-nonsensitive prey captured. The linear stabilimentum showed strong positive effects on the interception of large prey: webs with stabilimenta captured more than twice as many large prey (≥5?mm) than webs without stabilimenta, whereas there was only a slight difference in the interception rates for small prey (<5?mm). Comparisons among different Argiope species suggest that the stabilimentum may have different adaptive functions in different species or ecological contexts.     

Kleptoparasites: a twofold cost of group living for the colonial spider, Metepeira incrassata (Araneae, Araneidae)

Several species of kleptoparasitic and araneophagic spiders (Araneae: Family Theridiidae, Subfamily Argyrodinae) are found in colonial webs of the orb-weaving spider Metepeira incrassata (Araneae, Araneidae) from Mexico, where they steal food and/or prey upon their spider hosts. Census data from natural M. incrassata colonies reveal that the incidence of these species increases with colony size. This pattern may reflect the presence of several other orb-weaving spiders, each with their own kleptoparasitic species, invading larger M. incrassata colonies. As the number of these associated spiders increases, so does the density and number of Argyrodinae species in M. incrassata colonies, suggesting that associated spiders might reduce their own kleptoparasite load by building their webs within M. incrassata colonies. This represents a twofold cost to M. incrassata, as a field enclosure experiment revealed that a primarily kleptoparasitic species (Argyrodes elevatus) may reduce prey available to their hosts, but a kleptoparasitic/araneophagic species (Neospintharus concisus) inflicts high mortality upon M. incrassata. However, the cost of kleptoparasitism and predation by these species may be offset in part for M. incrassata individuals in large colonies by certain defensive mechanisms inherent in groups, i.e., “attack-abatement” and “selfish herd” effects. We conclude that increased occurrence of kleptoparasitic and/or predatory Argyrodinae spiders is a consequence of colonial web building and is an important potential cost of group living for colonial web-building spiders.     

Multiple techniques confirm elevational differences in insect size that may influence spider sociality

Social and subsocial spiders of the genus Anelosimus exhibit an altitudinal pattern in their geographic distribution at tropical latitudes in the Americas. Social species, which capture prey cooperatively, occur primarily in the lowland rain forest and are absent from higher elevations, whereas subsocial species are common at higher elevations but absent from the lowland rain forest. Previous studies have suggested that differences in the size of potential insect prey along altitudinal gradients may explain this pattern as insects were found to be, on average, larger in lowland rain forests than at higher elevations. These studies, however, may have under-sampled the insect size composition of each habitat because only one sampling technique was used. Using a number of collection methods we sampled the insect size composition in the environments of social and subsocial spiders in this genus. We found that the average insect size in lowland rain forest habitats was indeed larger than at high-elevation cloud forests in eastern Ecuador. We also found that, even though the various techniques differed in the size of the insects they captured (visual searching and blacklighting yielding larger insects than beating, sweeping, or malaise trapping), they all caught, on average, larger insects in the lowlands. Overall, spider colonies in the lowlands caught larger prey than did spider colonies at higher elevations, paralleling differences in insect size distribution obtained by the various techniques in their respective environments.     

The concentration of Cu and Pb in the funnel spider Eratigena atrica (C. L. Koch 1843) (Araneae: Agelenidae) and its web

Studies on the heavy metal concentrations on spider webs in relation to the pathways of pollution penetration (external and internal) have yet to be performed. This work assesses the concentration levels of two heavy metals: essential copper (Cu) and toxic lead (Pb) in spider webs and spiders (females, males and juveniles). Spiders divided into three treatment groups were exposed to the heavy metals in their diet as prey (fruit flies and mealworms larvae) were artificially contaminated with Cu and Pb. In general, we found higher rates of Cu compared to Pb concentrations in spiders and their webs. A positive correlation between levels of Cu and Pb in webs and spiders was found. Males had higher concentrations of both metals Cu and Pb in their bodies and webs compared to females. In an additional experiment, washed webs had significantly less metals than unwashed suggesting the dominance of external pollution in the contamination pathway.     

Agonistic interactions between male Frontinella pyramitela (Araneae,Linyphiidae)

Summary Adult male bowl and doily spiders, Frontinella pyramitela (Walckenaer) (Linyphiidae), occupy females' webs during courtship, mating, and foraging. When males are abundant, they can be found on about 20% of all adult females' webs, and encounters between the territorial resident males and intruder males occur frequently. Stereotyped interactions take place in 78% of encounters when the resident male has recently copulated on the web, though the presence of the female during the encounters has no effect. When the resident male has had no recent copulatory experience on the web, only 33% of encounters evoke visible stereotyped interaction.Analyses of videotaped interactions reveal that transitions from one behavior to another, though non-random, are highly variable (Fig. 1). The overall ordering of the interactions is species-typical with respect to the relative frequency of behavioral units and the relative amount of time spent in each one.Outcomes of the stereotyped interactions are very predictable: the larger male wins in 75% of all interactions, though when male sizes are closely matched, some significant resident advantage is detectable. A weak but significant inverse correlation between mass difference and duration of the jawlock display (Fig. 2) suggests that the display provides each male with information about his opponent's relative size.     

Influences of aggregative behaviour on space occupation in the spider Zygiella x-notata (Clerck)

Summary The distribution of the spider Zygiella x-notata was examined using field populations of adult females occupying the outside frames of windows. The structure of the populations was aggregative, and the distribution of individuals on the window frames and the size of the webs were density dependent. Also, the sizes of the webs of neighbouring spiders on the same window alternated. This spatial organization involves interactions between neighbours. If one spider out of two is removed, and if all the webs are destroyed, remaining spiders that previously had small webs significantly increase the size of their construction. In contrast, individuals that previously had large webs do not modify the size of their construction. This shows that individuals of Z. x-notata respond to the presence of neighbours. The influence of intraspecific interactions in such a population is discussed.     

Costs of courtship and mating in a sexually cannibalistic orb-web spider: female mating strategies and their consequences for males

The costs of courtship and mating may include increased risks of predation, the transmission of pathogens, and a loss of foraging opportunities. Thus, a female's decision to tolerate a courting male will depend upon how these costs offset the benefits of mating, which will depend on her reproductive and nutritional status. While these costs may be similar for mated and unmated females, the benefits of mating will be less for mated than virgin females. However, the cost of lost foraging opportunities may be higher for females with fewer nutritional reserves necessary for forming eggs. We examined how these costs and benefits influence the courtship and mating behaviour of male and female orb-web spiders, Argiope keyserlingi. In the field, females on webs that also contained a courting male intercepted fewer prey items per hour than females on webs without a male. In the laboratory, the presence of a courting male at the hub also attracted mantid predators to the web, increasing the risk of predation for both male and female. Staged mating experiments in the laboratory revealed that the frequency of female attacks and pre-copulatory cannibalism was greater among mated than virgin females. Feeding history did not affect aggression in virgin females but, among mated females, food-deprived spiders attacked and cannibalized males more frequently than sated females and only the latter ever remated. These differences in female behaviour influenced male mating strategies. Choice experiments demonstrated that males preferred to venture onto the silk threads of virgin rather than those of mated females. Similar patterns of mate selectivity were observed in the field; females with narrow abdomens attracted more males to the webs than females with broad abdomens, and copulations were observed more frequently among females with narrow abdomens. These smaller females are likely to be virgins that have recently molted. Males that preferentially mate with virgin females will not only avoid potentially fatal attacks but also obtain, on average, a higher fertilization success.     

Stingless bee response to spider webs is dependent on the context of encounter

In the course of their foraging bouts, bees frequently encounter spider webs among the vegetation. The ability to see and avoid these webs is vital for the success of the individual bee’s foraging bout. In this study, we report on the response of stingless bees (Trigona carbonaria) towards the webs of the St. Andrew’s Cross spider (Argiope keyserlingi). We studied the ability of bees to avoid webs in different contexts: when bees were on their foraging path or when they were returning to the hive as well as when they were flying North or South. We show that the probability of a bee being able to avoid a web depends on the context of the bee’s flight rather than the visual appearance of the web. Furthermore, the presence of the spider seems to alert the bee to the web, resulting in bees being more able to avoid capture. We show, specifically, that the probability of being captured is higher when the bee is returning to the hive compared with when the bee is foraging. The likelihood of avoiding a web is also influenced by the compass direction of the flight, although to a lesser extent. Our results indicate that the context of the predator–prey encounter has a significant influence on a bee’s ability to escape interception by a spider web.