David and Goliath: potent venom of an ant-eating spider (Araneae) enables capture of a giant prey

It is rare to find a true predator that repeatedly and routinely kills prey larger than itself. A solitary specialised ant-eating spider of the genus Zodarion can capture a relatively giant prey. We studied the trophic niche of this spider species and investigated its adaptations (behavioural and venomic) that are used to capture ants. We found that the spider captures mainly polymorphic Messor arenarius ants. Adult female spiders captured large morphs while tiny juveniles captured smaller morphs, yet in both cases ants were giant in comparison with spider size. All specimens used an effective prey capture strategy that protected them from ant retaliation. Juvenile and adult spiders were able to paralyse their prey using a single bite. The venom glands of adults were more than 50 times larger than those of juvenile spiders, but the paralysis latency of juveniles was 1.5 times longer. This suggests that this spider species possesses very potent venom already at the juvenile stage. Comparison of the venom composition between juvenile and adult spiders did not reveal significant differences. We discovered here that specialised capture combined with very effective venom enables the capture of giant prey.     

Prey detection without successful capture affects spider’s orb-web building behaviour

Animals obtain information from past foraging experience to adjust their foraging activity according to their environment. The ability of spiders to obtain information from unsuccessful predation experiences was investigated by examining the effects on web building, a significant foraging investment, of prey detection without successful capture in the orb-web spider Cyclosa octotuberculata. Four treatments were employed: (1) successful capture and feeding: one syrphid fly was allowed to be captured and consumed by the spider on the web; (2) single prey-item detection: a syrphid fly was placed on the web to lure the spider, but was removed before capture; (3) five prey-item detection: above prey-item detection stimulus was given five times; and, (4) control: neither prey nor feeding on the web. While control spiders decreased the total thread length and capture area of their webs, prey-item detection spiders in both conditions increased them, indicating that the spider obtained information from unsuccessful predation experience to adjust their foraging investment. The fed spiders exhibited a significantly greater increase than the prey-detection-only spiders, suggesting that prey detection alone and prey detection with consumption had different informational effects. Total thread length did not differ between single and five prey-item detection spiders, but distance between two adjacent sticky spirals increased only in the former spiders, possibly because five times unsuccessful predations prevented spiders to reduce web stickiness. It suggests that the spider changed web morphology according to the number of prey detection.     

Reverse positional orientation in a neotropical orb-web spider, <Emphasis Type="Italic">Verrucosa arenata</Emphasis>

Most orb-web spiders face downwards in the web. A downward orientation has been proposed to be the optimal strategy because spiders run faster downwards and thus can catch prey quicker. Consequently, orb-web spiders also extend their web in the lower part, leading to top-down web asymmetry. Since the majority of orb-web spiders face downwards, it has been difficult to test the effect of orientation on prey capture and web asymmetry. In this study, we explored the influence of reverse orientation on foraging efficiency and web asymmetry in Verrucosa arenata, a neotropical orb-web spider that faces upwards in the web. We show that reverse orientation does not imply reverse web asymmetry in this species. V. arenata spiders captured more prey in the lower part of the web but more prey per area on the upper part. The average running speeds of spiders did not differ between upward and downward running, but heavier spiders took longer to capture prey while running upwards. We discuss these findings in the context of foraging efficiency and web asymmetry.     

Selective olfactory attention of a specialised predator to intraspecific chemical signals of its prey

Prey-specialised predators have evolved specific cognitive adaptations that increase their prey searching efficiency. In particular, when the prey is social, selection probably favours the use of prey intraspecific chemical signals by predatory arthropods. Using a specialised ant-eating zodariid spider, Zodarion rubidum, which is known to prey on several ant species and possesses capture and venom adaptations more effective on Formicinae ants, we tested its ability to recognise chemical cues produced by several ant species. Using an olfactometer, we tested the response of Z. rubidum towards air with chemical cues from six different ant species: Camponotus ligniperda, Lasius platythorax and Formica rufibarbis (all Formicinae); and Messor structor, Myrmica scabrinodis and Tetramorium caespitum (all Myrmicinae). Z. rubidum was attracted to air carrying chemical cues only from F. rufibarbis and L. platythorax. Then, we identified that the spiders were attracted to airborne cues coming from the F. rufibarbis gaster and Dufour's gland, in particular. Finally, we found that among several synthetic blends, the decyl acetate and undecane mixture produced significant attraction of spiders. These chemicals are produced only by three Formicine genera. Furthermore, we investigated the role of these chemical cues in the communication of F. rufibarbis and found that this blend reduces their movement. This study demonstrates the chemical cognitive capacity of Z. rubidum to locate its ant prey using chemical signals produced by the ants. The innate capacity of Z. rubidum to olfactory detect different ant species is narrow, as it includes only two ant genera, confirming trophic specialisation at lower than subfamily level. The olfactory cue detected by Zodarion spiders is probably a component of the recruitment or trail pheromone.     

Loss of legs: is it or not a handicap for an orb-weaving spider?

Leg loss is a common phenomenon in spiders, and according to the species 5% to 40% of the adults can present at least one missing leg. There is no possibility of regeneration after adult moult and the animal must manage with its missing appendages until its death. With the loss of one or more legs, female orb-weaving spiders can be penalized twice: firstly, because the legs are necessary for web construction and secondly, the legs are essential for the control of the prey after its interception by the web. During development, spiders may be also penalized because regeneration has energetic costs that take away resources for survival, growth and reproduction. All these consequences should influence negatively the development of the spider and thus its fitness. We investigated the impact of leg loss in the orb-weaving spider, Zygiella x-notata by studying its frequency in a natural population and web building and prey capture behaviours in laboratory. In field populations, 9.5% to 13%, of the adult females presented the loss of one or more legs; the majority of individuals had lost only one leg (in 48% of cases, a first one). Leg loss seems to affect all the adult spiders, as there is no difference of mass between intact spiders and those with missing leg. Data obtained with laboratory-reared spiders, showed that the loss of legs due to the moult is rare (less than 1%). Considering changes in web design, spiders with missing legs decreased their silk investment, increased the distance between spiral turns but did not change the capture surface of the web. Under our laboratory experimental conditions, spiders with one or two lost legs did not present any difference in prey capture efficiency. In laboratory conditions, spiders with lost leg(s) did not show any difference in egg sac production or in longevity (adult lifespan) compared to intact spiders.     

Does ontogenetic change in orb web asymmetry reflect biogenetic law?

Most orb web spiders face downward on the web hub, and their webs are vertically asymmetrical, that is, the lower part of the web is larger than the upper part and the ratio of the lower part to the whole web area increases as the spider grows. This phenomenon may reflect biogenetic law such that young animals exhibit a general ancestral trait whereas adults exhibit specific and derived traits. An alternative explanation is that vertical asymmetry may arise from the difference in time required by spiders to move up or down the web to capture prey. The present study tested these two hypotheses for Eriophora sagana. Subadults of this species build their webs with reverse asymmetry in that the upper part of the web area is larger than the lower part. In both subadults and adults, the upper proportion decreased with spider weight, and adult spiders built more symmetric webs. These results support the capture time difference hypothesis.     

An estimated 400–800 million tons of prey are annually killed by the global spider community

Spiders have been suspected to be one of the most important groups of natural enemies of insects worldwide. To document the impact of the global spider community as insect predators, we present estimates of the biomass of annually killed insect prey. Our estimates assessed with two different methods suggest that the annual prey kill of the global spider community is in the range of 400–800 million metric tons (fresh weight), with insects and collembolans composing >90% of the captured prey. This equals approximately 1‰ of the global terrestrial net primary production. Spiders associated with forests and grasslands account for >95% of the annual prey kill of the global spider community, whereas spiders in other habitats are rather insignificant contributors over a full year. The spider communities associated with annual crops contribute less than 2% to the global annual prey kill. This, however, can be partly explained by the fact that annual crop fields are “disturbed habitats” with a low buildup of spider biomass and that agrobiont spiders often only kill prey over short time periods in a year. Our estimates are supported by the published results of exclusion experiments, showing that the number of herbivorous/detritivorous insects and collembolans increased significantly after spider removal from experimental plots. The presented estimates of the global annual prey kill and the relative contribution of spider predation in different biomes improve the general understanding of spider ecology and provide a first assessment of the global impact of this very important predator group.     

Context-dependent crypsis: a prey’s perspective of a color polymorphic predator

Many animals use body coloration as a strategy to communicate with conspecifics, prey, and predators. Color is a trade-off for some species, since they should be visible to conspecifics but cryptic to predators and prey. Some flower-dwelling predators, such as crab spiders, are capable of choosing the color of flowers where they ambush flower visitors and pollinators. In order to avoid being captured, visitors evaluate flowers visually before landing. The crab spider Mecaphesa dubia is a polymorphic species (white/purple color morphs), which inhabits the flower heads of a dune plant, Palafoxia lindenii. Using full-spectrum photography of spiders and flowers, we evaluated how honeybees perceived the spiders at different distances. Using visual modeling, we obtained the chromatic and achromatic contrasts of the spiders on flower heads as perceived by honeybees. Purple morphs were found mainly on the receptacle area and white morphs were equally likely to be found in the flowers and receptacle. According to theoretical modeling, white morphs were visible to honeybees from a distance of 10 cm in receptacle area but appeared to be cryptic in the flower area. Purple morphs were cryptic on the receptacle and less so when they were on the flowers. Spiders on flower heads are predicted to be more easily detected by honeybees using chromatic contrast. Our study shows that the conspicuousness of flower dwelling spiders to honeybees depends on the color morph, the distance of observation, and the position of spider on the flower head.     

Subsocial behaviour and brood adoption in mixed-species colonies of two theridiid spiders

Cooperation and group living often evolves through kin selection. However, associations between unrelated organisms, such as different species, can evolve if both parties benefit from the interaction. Group living is rare in spiders, but occurs in cooperative, permanently social spiders, as well as in territorial, colonial spiders. Mixed species spider colonies, involving closely related species, have rarely been documented. We examined social interactions in newly discovered mixed-species colonies of theridiid spiders on Bali, Indonesia. Our aim was to test the degree of intra- and interspecific tolerance, aggression and cooperation through behavioural experiments and examine the potential for adoption of foreign brood. Morphological and genetic analyses confirmed that colonies consisted of two related species Chikunia nigra (O.P. Cambridge, 1880) new combination (previously Chrysso nigra) and a yet undescribed Chikunia sp. Females defended territories and did not engage in cooperative prey capture, but interestingly, both species seemed to provide extended maternal care of young and indiscriminate care for foreign brood. Future studies may reveal whether these species adopt only intra-specific young, or also inter-specifically. We classify both Chikunia species subsocial and intra- and interspecifically colonial, and discuss the evolutionary significance of a system where one or both species may potentially benefit from mutual tolerance and brood adoption.     

Supercooling ability in the house spider, Achaearanea tepidariorum: effect of field-collected and laboratory-reared prey

The influence of prey animals on the supercooling ability of the house spider, Achaearanea tepidariorum, was studied by feeding spiders with field-collected and laboratory-cultured prey animals. Irrespective of the prey species supplied, spiders given field-collected prey had a higher supercooling point than those given laboratory-cultured counterparts. This means that (1) the field prey animals contained some efficient ice nucleators, whereas the laboratory animals were free from such substances and (2) the ice nucleators must be of external origin. Several lines of evidence also suggest that, under natural conditions, potential prey animals for the house spider are highly contaminated with ice nucleators.     

The hunter becomes the hunted: when cleptobiotic insects are captured by their target ants

Here we show that trying to rob prey (cleptobiosis) from a highly specialized predatory ant species is risky. To capture prey, Allomerus decemarticulatus workers build gallery-shaped traps on the stems of their associated myrmecophyte, Hirtella physophora. We wondered whether the frequent presence of immobilized prey on the trap attracted flying cleptoparasites. Nine social wasp species nest in the H. physophora foliage; of the six species studied, only Angiopolybia pallens rob prey from Allomerus colonies. For those H. physophora not sheltering wasps, we noted cleptobiosis by stingless bees (Trigona), social wasps (A. pallens and five Agelaia species), assassin bugs (Reduviidae), and flies. A relationship between the size of the robbers and their rate of capture by ambushing Allomerus workers was established for social wasps; small wasps were easily captured, while the largest never were. Reduviids, which are slow to extract their rostrum from prey, were always captured, while Trigona and flies often escaped. The balance sheet for the ants was positive vis-à-vis the reduviids and four out of the six social wasp species. For the latter, wasps began by cutting up parts of the prey’s abdomen and were captured (or abandoned the prey) before the entire abdomen was retrieved so that the total weight of the captured wasps exceeded that of the prey abdomens. For A. pallens, we show that the number of individuals captured during attempts at cleptobiosis increases with the size of the Allomerus’ prey.     

When attempts at robbing prey turn fatal

Because group-hunting arboreal ants spread-eagle insect prey for a long time before retrieving them, these prey can be coveted by predatory flying insects. Yet, attempting to rob these prey is risky if the ant species is also an effective predator. Here, we show that trying to rob prey from Azteca andreae workers is a fatal error as 268 out of 276 potential cleptobionts (97.1?%) were captured in turn. The ant workers hunt in a group and use the “Velcro?” principle to cling firmly to the leaves of their host tree, permitting them to capture very large prey. Exceptions were one social wasp, plus some Trigona spp. workers and flies that landed directly on the prey and were able to take off immediately when attacked. We conclude that in this situation, previously captured prey attract potential cleptobionts that are captured in turn in most of the cases.     

Biphasic activity of a jumping spider

Individual variation is a ubiquitous and important factor that affects ecological dynamics. This study examined individual variation in the nest-use pattern of the jumping spider Phidippus audax. Although the jumping spider is a diurnal species, field observations in this study revealed that the majority of individuals remained in their nests during the day. An accompanying examination of the hunger level of the spiders revealed that spiders that remained in nests were more starved than those observed outside nests. If spiders actively forage when they are starved, as has been suggested by previous studies, one would expect to see the opposite trend (i.e., spiders that remained in nests are more satiated). Thus, the pattern observed in the field contradicts the known behavioral pattern of the spiders. An individual-based model was used to investigate the behavioral mechanism of the spider and the discrepancy found in the observations. A basic assumption of the model is that spiders possess distinct inactive and active phases (biphasic activity pattern), and transitions between the two phases are regulated by the hunger level of the spider. Data from a laboratory experiment were used to examine the assumptions of the model partially. The model was able to capture patterns observed in the data, suggesting that the pattern of transitions in biphasic activity is an important trait of the foraging behavior of the jumping spider.     

Transmission of ice-nucleating active bacteria from a prey reduces cold hardiness of a predator (Araneae: Theridiidae)

The influence of ice-nucleating active (INA) bacteria on cold hardiness of the house spider, Achaearanea tepidariorum, was determined by measuring the supercooling point (SCP) of hatchlings given either INA-bacteria-fed or bacteria-free prey (Drosophila melanogaster). Spiders that had eaten INA-bacteria-fed flies showed higher SCPs than those fed on bacteria-free flies. Through feeding, INA bacteria in the prey reduce the cold hardiness of spiders. This fact should be taken into account before using INA agents as a means of pest management.     

Predation risk increases dispersal distance in prey

Understanding the ecological factors that affect dispersal distances allows us to predict the consequences of dispersal. Although predator avoidance is an important cause of prey dispersal, its effects on dispersal distance have not been investigated. We used simple experimental setups to test dispersal distances of the ambulatory dispersing spider mite (Tetranychus kanzawai) in the presence or absence of a predator (Neoseiulus womersleyi). In the absence of predators, most spider mites settled in adjacent patches, whereas the majority of those dispersing in the presence of predators passed through adjacent patches and settled in distant ones. This is the first study to experimentally demonstrate that predators induce greater dispersal distance in prey.     

Social spiders of the genus Anelosimus occur in wetter, more productive environments than non-social species

Latitude, rainfall, and productivity have been shown to influence social organisation and level of sociality in arthropods on large geographic scales. Social spiders form permanent group-living societies where they cooperate in brood care, web maintenance, and foraging. Sociality has evolved independently in a number of unrelated spider genera and may reflect convergent evolutionary responses to common environmental drivers. The genus Anelosimus contains a third of approximately 25 described permanently social spider species, eight to nine species that all occur in the Americas. To test for environmental correlates of sociality in Anelosimus across the Americas, we used logistic regression to detect effects of annual rainfall, productivity, and precipitation seasonality on the relative likelihood of occurrence of social and non-social Anelosimus spiders. Our analyses show that social species tend to occur at higher annual rainfall and productivity than non-social species, supporting the hypothesised effects of these environmental variables on the geographical distribution of social species. We did not find support for the hypothesis that permanently social species occur in areas with low precipitation seasonality. High annual precipitation and, to less extent, high productivity favour the occurrence of permanently group-living Anelosimus spiders relative to subsocial and solitary species. These results are partially consistent with previous findings for the Old World spider genus Stegodyphus, where a link between high habitat productivity and sociality was also found. Unlike Anelosimus, however, Stegodyphus typically occur in dry habitats negating a general importance of high precipitation for sociality. Sociality in spiders thus seems to be strongly linked to productivity, probably reflecting the need for relatively high availability of large prey to sustain social colonies.     

Grassy field margins and arthropod diversity: a case study on ground beetles and spiders in eastern Austria (Coleoptera: Carabidae; Arachnida: Aranei, Opiliones)

In 1983, the species composition and diversity of carabids, spiders and harvestmen was investigated by pitfall traps in a grassy field margin and in an adjacent, biologically farmed wheat field at Obere Lobau, Vienna, Austria.The carabid fauna of both habitats was diverse; it showed a high degree of similarity, the abundant species in both habitats being represented by typical field species. Only Metophonus spp. predominantly lived in the margin. Numerous species of different habitat origin occurred in the margin at low abundances indicating transitional stay rather than permanent populations.In contrast, the spider fauna showed a low degree of similarity, with few agrobiotic species strongly dominating field fauna. In the field margin, a rich spider fauna containing rare elements indicates the general importance of grassy margins for nature conservation. The apparently low faunal exchange of spiders between the two habitat types is discussed. Harvestmen occurred mainly in the field margin; only two thermophilic species invaded the field.Seasonal fluctuations in the trapping numbers of Bembidion lampros, Platynus dorsalis and Brachinus explodens are interpreted as indicating migrations between field margin and field. Poecilus cupreus and certain other field species, however, apparently spend their entire life cycle in the field. The possible function of field margins for restoration of carabid losses due to impacts of intensive cultivation is discussed.It is concluded that both grassy field margins and sustainable farming methods, in particular biological farming, are necessary to maintain a diverse predatory arthropod fauna in agroecosystems.     

Adjustment of web-building initiation to high humidity: a constraint by humidity-dependent thread stickiness in the spider Cyrtarachne

Cyrtarachne is an orb-weaving spider belonging to the subfamily Cyrtarachninae (Araneidae) which includes triangular-web-building Pasilobus and bolas spiders. The Cyrtarachninae is a group of spiders specialized in catching moths, which is thought to have evolved from ordinary orb-weaving araneids. Although the web-building time of nocturnal spiders is in general related to the time of sunset, anecdotal evidence has suggested variability of web-building time in Cyrtarachne and its closely related genera. This study has examined the effects of temperature, humidity, moonlight intensity, and prey (moths) availability on web-building time of Cyrtarachne bufo, Cyrtarachne akirai, and Cyrtarachne nagasakiensis. Generalized linear mixed model (GLMM) have revealed that humidity, and not prey availability, was the essential variable that explained the daily variability of web-building time. Experiments measuring thread stickiness under different humidities showed that, although the thread of Cyrtarachne was found to have strong stickiness under high humidity, low humidity caused a marked decrease of thread stickiness. By contrast, no obvious change in stickiness was seen in an ordinary orb-weaving spider, Larinia argiopiformis. These findings suggest that Cyrtarachne adjusts its web-building time to favorable conditions of high humidity maintaining strong stickiness, which enables the threads to work efficiently for capturing prey.     

Dietary and prey-capture adaptations by which <Emphasis Type="Italic">Zodarion germanicum</Emphasis>, an ant-eating spider (Araneae: Zodariidae), specialises on the Formicinae

There has been considerable recent interest in the biology of spiders that specialise on ants as prey, but previous studies have tended to envisage the level of adaptation as being to ants as a group. In this paper, we provide evidence that Zodarion germanicum is a spider that has dietary and venom adaptations by which it targets a particular subset of ants, the subfamily Formicinae. We reared spiders from first instar in the laboratory on three different diets: formicine ants only, myrmicine ants only and mixed (both formicine and myrmicine ants). Fitness-related life-history parameters were determined, and we found that the spiders on the formicine-only diet lived longer and grew at a faster rate. Lipid, carbon and nitrogen compositions of ants were analysed, but we found no evidence of formicines differing from myrmicines in macro-nutrient content. This suggests that effects on longevity and growth depended on more specific nutrients or on compounds the prey uses for defence. We investigated how efficient Z. germanicum was at paralysing different ants and our findings suggest that the spider's venom is especially effective against formicines. Taken together, our findings suggest that Z. germanicum has evolved specialisation at the level of targeting a particular ant subfamily, the Formicinae.     

Altruism during predation in an assassin bug

Zelus annulosus is an assassin bug species mostly noted on Hirtella physophora, a myrmecophyte specifically associated with the ant Allomerus decemarticulatus known to build traps on host tree twigs to ambush insect preys. The Z. annulosus females lay egg clutches protected by a sticky substance. To avoid being trapped, the first three instars of nymphs remain grouped in a clutch beneath the leaves on which they hatched, yet from time to time, they climb onto the upper side to group ambush preys. Long-distance prey detection permits these bugs to capture flying or jumping insects that alight on their leaves. Like some other Zelus species, the sticky substance of the sundew setae on their forelegs aids in prey capture. Group ambushing permits early instars to capture insects that they then share or not depending on prey size and the hunger of the successful nymphs. Fourth and fifth instars, with greater needs, rather ambush solitarily on different host tree leaves, but attract siblings to share large preys. Communal feeding permits faster prey consumption, enabling small nymphs to return sooner to the shelter of their leaves. By improving the regularity of feeding for each nymph, it likely regulates nymphal development, synchronizing molting and subsequently limiting cannibalism.