Armoured spiderman: morphological and behavioural adaptations of a specialised araneophagous predator (Araneae: Palpimanidae)

In a predator–prey system where both intervenients come from the same taxon, one can expect a strong selection on behavioural and morphological traits involved in prey capture. For example, in specialised snake-eating snakes, the predator is unaffetced by the venom of the prey. We predicted that similar adaptations should have evolved in spider-eating (araneophagous) spiders. We investigated potential and actual prey of two Palpimanus spiders (P. gibbulus, P. orientalis) to support the prediction that these are araneophagous predators. Specific behavioural adaptations were investigated using a high-speed camera during staged encounters with prey, while morphological adaptations were investigated using electron microscopy. Both Palpimanus species captured a wide assortment of spider species from various guilds but also a few insect species. Analysis of the potential prey suggested that Palpimanus is a retreat-invading predator that actively searches for spiders that hide in a retreat. Behavioural capture adaptations include a slow, stealthy approach to the prey followed by a very fast attack. Morphological capture adaptations include scopulae on forelegs used in grabbing prey body parts, stout forelegs to hold the prey firmly, and an extremely thick cuticle all over the body preventing injury from a counter bite of the prey. Palpimanus overwhelmed prey that was more than 200% larger than itself. In trials with another araneophagous spider, Cyrba algerina (Salticidae), Palpimanus captured C. algerina in more than 90% of cases independent of the size ratio between the spiders. Evidence indicates that both Palpimanus species possesses remarkable adaptations that increase its efficiency in capturing spider prey.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Mass predicts web asymmetry in Nephila spiders

The architecture of vertical aerial orb webs may be affected by spider size and gravity or by the available web space, in addition to phylogenetic and/or developmental factors. Vertical orb web asymmetry measured by hub displacement has been shown to increase in bigger and heavier spiders; however, previous studies have mostly focused on adult and subadult spiders or on several size classes with measured size parameters but no mass. Both estimations are suboptimal because (1) adult orb web spiders may not invest heavily in optimal web construction, whereas juveniles do; (2) size class/developmental stage is difficult to estimate in the field and is thus subjective, and (3) mass scales differently to size and is therefore more important in predicting aerial foraging success due to gravity. We studied vertical web asymmetry in a giant orb web spider, Nephila pilipes, across a wide range of size classes/developmental stages and tested the hypothesis that vertical web asymmetry (measured as hub displacement) is affected by gravity. On a sample of 100 webs, we found that hubs were more displaced in heavier and larger juveniles and that spider mass explained vertical web asymmetry better than other measures of spider size (carapace and leg lengths, developmental stage). Quantifying web shape via the ladder index suggested that, unlike in other nephilid taxa, growing Nephila orbs do not become vertically elongated. We conclude that the ontogenetic pattern of progressive vertical web asymmetry in Nephila can be explained by optimal foraging due to gravity, to which the opposing selective force may be high web-building costs in the lower orb. Recent literature finds little support for alternative explanations of ontogenetic orb web allometry such as the size limitation hypothesis and the biogenetic law.     

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.     

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.     

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.     

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.     

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.     

Cross-habitat variation in the phenology of a colonial spider: insights from a reciprocal transplant study

In species with widespread distribution, populations found in markedly different environments can show differences in developmental traits. This, in time, can have an effect on reproductive success. Sources of variation in developmental traits can be genetic or environmentally induced. I examined the relationship between environmental and genetic influences on juvenile development in populations of the colonial spider, Parawixia bistriata, located at sites with different moisture regimes and associated environmental variables (e.g., prey availability). It was expected that individuals from different populations would show differences in developmental traits and that those differences will be associated with lower reproductive success at dry sites. I recorded the phenology and developmental traits of native and transplanted individuals in the field and estimated reproductive success based on clutch size. Colonies from wet versus dry sites showed different phenologies, with individuals at dry sites maturing later. Transplant results suggest plasticity in instar duration caused by environmental effects. Despite differences in resources and spider phenology, clutch sizes of native dry and wet populations were similar. Transplanted individuals, however, were differentially affected. Transplants from wet to dry sites (WD) showed lower growth rates and smaller clutches, whereas transplants from dry to wet sites had larger clutch sizes than in native habitat. Delayed maturation and failure to reproduce in WD individuals is associated with a lower tendency to capture prey in groups and less aggressive interactions during prey capture. Thus, despite negative environmental effects on development, dry native individuals have evolved non-developmental traits that allow successful reproduction.     

Optimal web investment in sub-optimal foraging conditions

Orb web spiders sit at the centre of their approximately circular webs when waiting for prey and so face many of the same challenges as central-place foragers. Prey value decreases with distance from the hub as a function of prey escape time. The further from the hub that prey are intercepted, the longer it takes a spider to reach them and the greater chance they have of escaping. Several species of orb web spiders build vertically elongated ladder-like orb webs against tree trunks, rather than circular orb webs in the open. As ladder web spiders invest disproportionately more web area further from the hub, it is expected they will experience reduced prey gain per unit area of web investment compared to spiders that build circular webs. We developed a model to investigate how building webs in the space-limited microhabitat on tree trunks influences the optimal size, shape and net prey gain of arboricolous ladder webs. The model suggests that as horizontal space becomes more limited, optimal web shape becomes more elongated, and optimal web area decreases. This change in web geometry results in decreased net prey gain compared to webs built without space constraints. However, when space is limited, spiders can achieve higher net prey gain compared to building typical circular webs in the same limited space. Our model shows how spiders optimise web investment in sub-optimal conditions and can be used to understand foraging investment trade-offs in other central-place foragers faced with constrained foraging arenas.     

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.     

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.     

Silk wrapping of nuptial gifts as visual signal for female attraction in a crepuscular spider

An extensive diversity of nuptial gifts is known in invertebrates, but prey wrapped in silk is a unique type of gift present in few insects and spiders. Females from spider species prefer males offering a gift accepting more and longer matings than when males offered no gift. Silk wrapping of the gift is not essential to obtain a mating, but appears to increase the chance of a mating evidencing a particularly intriguing function of this trait. Consequently, as other secondary sexual traits, silk wrapping may be an important trait under sexual selection, if it is used by females as a signal providing information on male quality. We aimed to understand whether the white color of wrapped gifts is used as visual signal during courtship in the spider Paratrechalea ornata. We studied if a patch of white paint on the males’ chelicerae is attractive to females by exposing females to males: with their chelicerae painted white; without paint; and with the sternum painted white (paint control). Females contacted males with white chelicerae more often and those males obtained higher mating success than other males. Thereafter, we explored whether silk wrapping is a condition-dependent trait and drives female visual attraction. We exposed good and poor condition males, carrying a prey, to the female silk. Males in poor condition added less silk to the prey than males in good condition, indicating that gift wrapping is an indicator of male quality and may be used by females to acquire information of the potential mate.