Bolas Spiders Research Articles

Behavior and Bioadhesives: How Bolas Spiders, Mastophora hutchinsoni, Catch Moths.

Spiders use various combinations of silks, adhesives, and behaviors to ensnare and trap prey. A common but difficult to catch prey in most spider habitats are moths. They easily escape typical orb-webs because their bodies are covered in sacrificial scales that flake off when in contact with the web's adhesives. This defense is defeated by spiders of the sub-family of Cyrtarachninae, moth-catching specialists who combine changes in orb-web structure, predatory behavior, and chemistry of the aggregate glue placed in those webs. The most extreme changes in web structure are shown by bolas spiders, who create a solitary capture strand containing only one or two glue droplets at the end of a single thread. They prey on male moths by releasing pheromones to draw them within range of their bolas, which they flick to ensnare the moth. We used a high-speed video camera to capture the behavior of the bolas spider Mastophora hutchinsoni. We calculated the kinematics of spiders and moths in the wild to model the physical and mechanical properties of the bolas during prey capture, the behavior of the moth, and how these factors lead to successful prey capture. We created a numerical model to explain the mechanical behavior of the bolas silk during prey capture. Our kinematic analysis shows that the material properties of the aggregate glue bolas of M. hutchinsoni are distinct from that of the other previously analyzed moth-specialist, Cyrtarachne akirai. The spring-like behavior of the M. hutchinsoni bolas suggests it spins a thicker liquid.

Mechanics of the Prey Capture Technique of the South African Grassland Bolas Spider, Cladomelea akermani.

Spiders use various combinations of silks, adhesives, and behaviors to ensnare prey. One common but difficult-to-catch prey is moths. They easily escape typical orb-webs because their bodies are covered in tiny sacrificial scales that flake off when in contact with the web's adhesives. This defense is defeated by spiders of the sub-family of Cyrtarachninae-moth-catching specialists who combine changes in orb-web structure, predatory behavior, and chemistry of the aggregate glue placed in those webs. The most extreme changes in web structure are shown by the bolas spiders which create only one or two glue droplets at the end of a single thread. They prey on male moths by releasing pheromones to draw them close. Here, we confirm the hypothesis that the spinning behavior of the spider is directly used to spin its glue droplets using a high-speed video camera to observe the captured behavior of the bolas spider Cladomelea akermani as it actively spins its body and bolas. We use the kinematics of the spider and bolas to begin to quantify and model the physical and mechanical properties of the bolas during prey capture. We then examine why this species chooses to spin its body, an energetically costly behavior, during prey capture. We test the hypothesis that spinning helps to spread pheromones by creating a computational fluid dynamics model of airflow within an open field and comparing it to that of airflow within a tree, a common environment for bolas spiders that do not spin. Spinning in an open environment creates turbulent air, spreading pheromones further and creating a pocket of pheromones. Conversely, spinning within a tree does little to affect the natural airflow.

Repeat Variation Resolves a Complete Aggregate Silk Sequence of Bolas Spider Mastophora phrynosoma.

Many species of spider use a modified silk adhesive, called aggregate glue, to aid in prey capture. Aggregate spidroins (spider fibroins) are modified members of the spider silk family; however, they are not spun into fibers as are their solid silk relatives. The genes that encode for aggregate spidroins are the largest of the known spidroin genes and are similarly highly repetitive. In this study, we used long read sequencing to discover the aggregate spidroin genes of the toad-like bolas spider, Mastophora phrynosoma, which employs the glue in a unique way, using only a single, large droplet to capture moths. While Aggregate Spidroin 1 (AgSp1) remains incomplete, AgSp2 is more than an extraordinary 62 kb of coding sequence, 20 kb longer than the longest spidroin on record. The structure of repeats from both aggregate silk proteins follows a similar pattern seen in other species, with the same strict conservation of amino acid residue number for much of the repeats' lengths. Interestingly, AgSp2 lacks the elevated number and groupings of glutamine residues seen in the other reported AgSp2 of a classic orb weaving species. The role of gene length in glue functionality remains a mystery, and thus discovering length differences across species will allow understanding and harnessing of this attribute for the next generation of bio-inspired adhesives.

New records of Cladomelea from South Africa, including the first records of C. longipes (O. Pickard-Cambridge, 1877) (Araneae, Araneidae) outside its type locality

We present the first records of the bolas spider, Cladomelea longipes (O. Pickard-Cambridge, 1877), beyond its type locality, resulting in a considerable extension of its geographic range in Africa. We compare C. longipes with the two other species of Cladomelea known from South Africa, C. akermani Hewitt, 1923 and C. debeeri Roff & Dippenaar-Schoeman, 2004. Images of live specimens and a distribution map are provided. Cladomelea longipes is very rare locally but has a relatively large geographical distribution in the Afrotropical Region.

Deceptive signals and behaviors of a cleptoparasitic beetle show local adaptation to different host bee species

Chemosensory signals play a key role in species recognition and mate location in both invertebrate and vertebrate species. Closely related species often produce similar but distinct signals by varying the ratios or components in pheromone blends to avoid interference in their communication channels and minimize cross-attraction among congeners. However, exploitation of reproductive signals by predators and parasites also may provide strong selective pressure on signal phenotypes. For example, bolas spiders mimic the pheromones of several moth species to attract their prey, and parasitic blister beetle larvae, known as triungulins, cooperatively produce an olfactory signal that mimics the sex pheromone of their female host bees to attract male bees, as the first step in being transported by their hosts to their nests. In both cases, there is strong selection pressure on the host to discriminate real mates from aggressive mimics and, conversely, on the predator, parasite, or parasitoid to track and locally adapt to the evolving signals of its hosts. Here we show local adaptation of a beetle, Meloe franciscanus (Coleoptera: Meloidae), to the pheromone chemistry and mate location behavior of its hosts, two species of solitary bees in the genus Habropoda We report that Mfranciscanus' deceptive signal is locally host-adapted in its chemical composition and ratio of components, with host bees from each allopatric population preferring the deceptive signals of their sympatric parasite population. Furthermore, in different locales, the triungulin aggregations have adapted their perching height to the height at which local male bees typically patrol for females.

Unusual Microstructure and Mechanical Properties of Egg Case of the Bolas Spider Mastophora corpulenta Banks (Araneae, Araneidae)

Bolas spiders of the genus Mastophora are very uncommon orb-weaver spiders, famous for their unusual predatory behavior. Being strictly nocturnal and very cryptic, they are extremely difficult to reveal, which explains their rarity in world arachnological collections. After a recent finding of an adult female of Mastophora corpulenta Banks (one of especially rare representatives of the genus), a few egg cases of this species became available, which seem to be very different from those of more common spiders due to their unusual hardness and coloration. We characterized some spectral, structural, and mechanical properties of this unusual silk material, by using Fourier-transform infrared spectroscopy, scanning electron microscopy (SEM), 3D profilometer imaging, and atomic force microscopy (AFM). For comparison, similar studies were performed for egg cases of the Southern black widow Latrodectus mactans Fabricius, since spiders of the genus Latrodectus are known to produce silk fibers of comparable toughness. Some similarities were observed between the silks produced by Mastophora corpulenta and Latrodectus mactans in terms of the size and chemical composition of egg cases. At the same time, SEM imaging and AFM force characterization revealed striking differences between them, due to the fact that Mastophora egg cases, unlike those produced by more common Araneae species, includes a solid (fused) wall, lacking evident porous structure, which results in their outstanding stiffness and strength.

Experimental evidence that high humidity is an essential cue for web building in Pasilobus spiders

Spiders in the subfamily Cyrtarachninae, including bolas spiders, are moth specialists, and it has been suggested that these spiders initiate web-weaving under high humidity. Here we used Pasilobus hupingensis to experimentally test whether Cyrtarachninae spiders build webs exclusively under high humidity. The results showed that humidity, as well as temperature and prey feeding history, affected web-building probability, but humidity had a much stronger effect. Moreover, spiders never constructed webs at under <70% humidity. We suggest that a mechanical property in sticky materials derived from moth specialization; namely, unusually high, yet rapidly degrading stickiness, is likely to have promoted the evolution of plastic foraging behaviour that varies with humidity.

Luring

Bulbert and Wignall introduce the ways animals lure their prey.

Molecular phylogeny of moth-specialized spider sub-family Cyrtarachninae, which includes bolas spiders.

The evolutionary process of the unique web architectures of spiders of the sub-family Cyrtarachninae, which includes the triangular web weaver, bolas spider, and webless spider, is thought to be derived from reduction of orbicular 'spanning-thread webs' resembling ordinal orb webs. A molecular phylogenetic analysis was conducted to explore this hypothesis using orbicular web spiders Cyrtarachne, Paraplectana, Poecilopachys, triangular web spider Pasilobus, bolas spiders Ordgarius and Mastophora, and webless spider Celaenia. The phylogeny inferred from partial sequences of mt-COI, nuclear 18S-rRNA and 28S-rRNA showed that the common ancestor of these spiders diverged into two clades: a spanning-thread web clade and a bolas or webless clade. This finding suggests that the triangular web evolved by reduction of an orbicular spanning web, but that bolas spiders evolved in the early stage, which does not support the gradual web reduction hypothesis.

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.

Sex Pheromone Components of the Bronzed Cutworm, Nephelodes minians, a Prey Species of a Bolas Spider, Mastophora hutchinsoni

The bolas spider, Mastophora hutchinsoni, attracts adult males of four species of moths by aggressively mimicking their sex pheromone. Here, we report the identification of two sex pheromone components of one of these species, the bronzed cutworm, Nephelodes minians. Simultaneous gas chromatographic (flame ionization detection) and electroantennographic detection (EAD) analysis of extracts of the sex pheromone glands of female N. minians indicated two components eliciting strong EAD responses from a conspecific male antenna that corresponded in retention time with (Z)-11-hexadecenal (Z11-16:Ald) and (Z)-11-hexadecenyl acetate (Z11-16:OAc), using both polar and nonpolar columns. Mass spectra of these two peaks were identical to those of synthetic Z11-16:Ald and Z11-16:OAc. The double-bond positions were confirmed by GC-MS analysis of dimethyl disulfide derivatives of the putative pheromone components. In a field test, a 5:1 blend of Z11-16:Ald to Z11-16:OAc attracted male N. minians. Overall, there is no overlap in the chemical constituents of the sex pheromones of three moth species preyed upon by this bolas spider for which pheromones have now been identified. These studies suggest that bolas spiders are versatile in their ability to synthesize semiochemicals for different prey species. This versatility may be advantageous to a predator that has an otherwise extremely specialized hunting tactic.

Aggressive chemical mimicry of moth pheromones by a bolas spider: how does this specialist predator attract more than one species of prey?

The bolas spider, Mastophora hutchinsoni, attracts Lacinipolia renigera and Tetanolita mynesalis males by mimicking the female moth sex pheromones. However, as the prey species use completely different pheromone blends we conducted experiments to determine how this is accomplished by the predator. The periodicity of L. renigera mate-seeking activities occurs early in the scotophase, whereas male T. mynesalis are active late at night, corresponding with periods when these moths are captured by the spider. The pheromone blend of early-flying L. renigera interferes with attraction of late-flying T. mynesalis to its pheromone in a dose-dependent manner, suggesting the spider must always produce a single sub-optimal “compromise” blend for both species or that it adjusts its allomonal blend to optimize capture of the respective prey species at different times during the night. We delayed (L. renigera) or advanced (T. mynesalis) the periodicity of male activity through photoperiodic manipulation and found that the bolas spider attracted both prey species outside their normal activity windows. These results support the idea that bolas spiders produce components of both species at all times rather than producing the pheromone of each prey species at different times of the night. However, using coupled gas chromatography-electroantennography, we also demonstrated that the spider decreases its emission of the L. renigera pheromone over the course of the night. This modification should reduce the behavioral antagonism of the L. renigera pheromone on T. mynesalis males and increase the predator's success of attracting T. mynesalis during this prey's normal activity window late at night.

ムツトゲイセキグモの生活史および「投げ縄」作成と餌捕獲行動

Ordgarius sexspinosus (Araneae: Araneidae) is one of the two bolas spiders in Japan. This report documents phenology, hunting behavior of newly emerged spiderlings, and the construction of bolas by subadult and adult females of O. sexspinosus. Ordgarius sexspinosus is univoltine, overwinters in the nymphal stages inside egg sac, and the female produced 3-6 egg sacs. Spiderlings of earlier stages and males did not make bolas during their perching at the leaf margins. Subadult and adult females employed bolas to capture moths. The behavior of bolas construction was very similar to that of the genus Mastophora, except that it holds the bolas thread by a second leg instead of a first leg. The bolas sometimes consisted of two different sticky balls.

Detection of prey by a spider that aggressively mimics pheromone blends

Adult female bolas spiders have a unique hunting tactic that combines aggressive chemical mimicry of the sex pheromone blends of their prey moths with a specialized weapon (the bolas) and behaviors to capture attracted male moths. This report shows that female bolas spiders can release the attractive allomone before they make the bolas and that females detect moth wing vibrations from attracted prey. In response to this detection, females initiate the construction of a bolas. This ability to sample for prey presence may allow this predator to adapt its hunting activity to the temporal and spatial availability of its prey and, thereby, may reduce the constraints associated with extreme prey specialization.

Extraordinary web and silk properties of Cyrtarachne (Araneae, Araneidae): a possible link between orb-webs and bolas

Cyrtarachne is an orb-weaving spider of the sub-family Cyrtarachninae (Araneidae), which includes the triangle-web-building Pasilobus and the bolas spiders. We found that web and thread characteristics of Cyrtarachne differed greatly from those of typical orb-webs. Web diameter, sticky spiral spacing, breaking strength and stickiness of thread, thread diameter and droplet diameter were significantly different from those of other members of Araneidae. It is especially worth noting that the diameter was approximately four times, and the breaking strength seven to ten times larger in Cyrtarachne viscid threads than in those of other araneids. Kinetic energy-absorbing ability of Cyrtarachne threads was much greater than in that of other species, and close to the amount of kinetic energy generated by flying moths. Viscid material of threads was peculiar because its adhesiveness decreased to zero in a few hours. Moreover, SEM photos revealed them to be covered with thin scales of material, while threads of other araneids were smooth. These two facts suggest that the viscid material of Cyrtarachne threads may be different from those of other orb-weavers. As web-building, hunting behaviour and prey composition of different species of Cyrtarachninae arc quite similar to each other, we hypothesize that these extraordinary web and thread characteristics of Cyrtarachne are shared by the other members of this sub-family. Because these characteristics differ in many ways from those of typical araneid orb-webs, there appears to have been a great leap in evolution between Cyrtarachne and the other Araneidae.

Extraordinary web and silk properties of Cyrtarachne (Araneae, Araneidae): a possible link between orb-webs and bolas

Cyrtarachne is an orb-weaving spider of the sub-family Cyrtarachninae (Araneidae), which includes the triangle-web-building Pasilobus and the bolas spiders. We found that web and thread characteristics ofCyrtarachne differed greatly from those of typical orb-webs. Web diameter, sticky spiral spacing, breaking strength and stickiness of thread, thread diameter and droplet diameter were significantly different from those of other members of Araneidae. It is especially worth noting that the diameter was approximately four times, and the breaking strength seven to ten times larger in Cyrtarachne viscid threads than in those of other araneids. Kinetic energy-absorbing ability of Cyrtarachne threads was much greater than in that of other species, and close to the amount of kinetic energy generated by flying moths. Viscid material of threads was peculiar because its adhesiveness decreased to zero in a few hours. Moreover, SEM photos revealed them to be covered with thin scales of material, while threads of other araneids were smooth. These two facts suggest that the viscid material of Cyrtarachne threads may be different from those of other orb-weavers. As web-building, hunting behaviour and prey composition of different species of Cyrtarachninae are quite similar to each other, we hypothesize that these extraordinary web and thread characteristics of Cyrtarachne are shared by the other members of this sub-family. Because these characteristics differ in many ways from those of typical araneid orb-webs, there appears to have been a great leap in evolution between Cyrtarachne and the other Araneidae.

Aggressive Chemical Mimicry by the Bolas Spider Mastophora hutchinsoni: Identification and Quantification of a Major Prey's Sex Pheromone Components in the Spider's Volatile Emissions

The adult female bolas spider Mastophora hutchinsoni feeds exclusively on attracted males of a few moth species. This exclusivity and the behavior of the approaching moths suggest that the spider aggressively mimics the sex pheromones of its prey species. Males of the bristly cutworm, Lacinipolia renigera, are a major prey of this spider, accounting for about two thirds of the biomass of prey consumed. Female bristly cutworms produce a pheromone blend consisting of (Z)-9-tetradecenyl acetate (Z9–14 : Ac) and (Z,E)-9,12-tetradecenyl acetate (ZE-9,12–14 : Ac). To determine if M. hutchinsoni females mimic the sex pheromone components and blend ratio of L. renigera, we collected volatiles from hunting adult female spiders and analyzed them with gas chromatography–electroantennographic detection (GC-EAD) and gas chromatography–mass spectrometry (GC-MS). GC-EAD analysis of volatile collections, using a male bristly cutworm antenna as the detector and two capillary columns of different polarities, revealed the presence of peaks with retention times (Rts) identical to Z9–14 : Ac and ZE-9,12– 14 : Ac. The mass spectrum of a peak with Rt of Z9–14 : Ac was identical to the mass spectrum of the synthetic equivalent. There was an insufficient quantity of the compound with Rt of ZE-9,12–14 : Ac to get a full spectrum, but selective detection of ions at m/z 61 and 192 at the correct Rt supported the identification. On average, the blend collected from spiders contained 54.8 ± 20.8 (SE) pg/min of Z9–14 : Ac and 2.5 ± 1.7 (SE) pg/min of ZE-9,12–14 : Ac. The latter, on average, comprised 2.6 ± 0.7% of the total, which is similar to the blend ratio emitted by bristly cutworm females. Our results indicate that the adult female M. hutchinsoni produces an allomone blend that mimics not only the composition, but also the blend ratio, of the sex pheromone of a major prey species.

Exploitation of Intraspecific Communication Systems: Illicit Signalers and Receivers

We review exploitation of intraspecific communication by illicit signalers or receivers, restricting coverage to examples in which the exploiter or exploited, or both, is an arthropod. Illicit signalers aggressively mimic the chemical, acoustical, or visual signals normally used by their victims in sexual or social communication. Cited examples include bolas spiders that mimic pheromone blends to attract male moths as prey and femme fatale fireflies that mimic the flashing pattern of other species of fireflies to prey upon the responding males. Illicit receivers gain access to resources by eavesdropping on intraspecific signals. For example, several species of predatory beetles respond to the aggregation pheromones of bark beetles to feed on them or their offspring, and some parasitic flies orient to the stridulation songs of orthopteran species. In some cases, functional intraspecific communication systems may have evolved to reduce exploitation by illicit receivers; for example, changes in signal characteristics could make the signaler less apparent to potential exploiters. With rare exceptions, both illicit signalers and receivers tend to exploit the intraspecific communication systems of a limited number of taxa, probably because the production or detection of species-specific signals often requires the evolution of specialized signaling mechanisms or sensitive receptors. To convincingly demonstrate exploitation of intraspecific communication, one must first decipher the signals and responses that are part of the communication system. To date, the intraspecific communication systems of a few taxa (e.g., Lepidoptera, fireflies, crickets) are reasonably well understood, but those of many other groups are unknown or poorly understood. Even with this limitation, it is clear that exploitation of these systems by illicit signalers and receivers is widespread and diverse.

Adult male bolas spiders retain juvenile hunting tactics.

Bolas spiders in the genus Mastophora exhibit extreme sexual size dimorphism. In temperate regions, the diminutive males become adults about 2 months before females mature. Late-instar and adult females attract certain male moths by aggressive chemical mimicry of those moth species' sex pheromones. While hunting, these larger female spiders hang from a horizontal silken line and capture moths by swinging a "bolas" (i.e., a sticky globule suspended on a thread) at the approaching moths. Small, early-instar bolas spiders of both sexes attract moth flies in the genus Psychoda, which they capture without using a bolas or web. Instead, they position themselves along leaf margins and use their front two pairs of legs to grab approaching prey. The predatory habits of adult male bolas spiders have never been reported. Our field experiments demonstrated that adult males of the bolas spider Mastophora phrynosoma attract adult male Psychoda phalaenoides. Each year during our 3-year study, significantly more P. phalaenoides were captured on sticky traps baited with live adult male M. phrynosoma than on unbaited control traps. Thus, the tiny adult male bolas spiders retain the juvenile hunting tactic of attracting psychodid flies, while female bolas spiders switch from hunting psychodid flies as spiderlings to hunting moths when the female spiders become older and larger.

Identification of sex pheromone ofTetanolita mynesalis (Lepidoptera: Noctuidae), a prey species of bolas spider,Mastophora hutchinsoni

The bolas spider,Mastophora hutchinsoni, attracts adult males of four species of nocturnally active Lepidoptera through aggressive chemical mimicry of those species' sex pheromones. Here we report the identification of the sex pheromone of one prey species, the smoky tetanolita (Tetanolita mynesalis). In sex pheromone gland extracts, only two peaks stimulated an electrophysiological response as measured by a coupled gas chromatography-electroantennographic detection analysis. These two peaks had retention times identical to (3Z,6Z,9Z)-heneicosatriene (3Z,6Z,9Z-21:H) and (3Z,9Z)-cis-6,7-epoxy-heneicosadiene (3Z,9Z-cis-6,7-epoxy-21:H), respectively, and mass spectra identical to these two compounds. It was determined that 0.23±0.16 and 0.56±0.26 ng of 3Z,6Z,9Z-21:H and 3Z,9Z-cis-6,7-epoxy-21:H, respectively, were present in pheromone gland extracts from individual females. A 1:1 blend of 3Z,6Z,9Z-21:H and 3Z,9Z-6S,7R-epoxy-21:H was an effective attractant for adult males from feral populations. Blend ratios of these two components from 2:1 to 1:2 were equally effective as attractants. Greater deviation from the optimal blends resulted in diminished trap catches. The enantiomer 3Z,9Z-6R,7S-epoxy-21:H not only was not effective in attracting males, its presence in the effective blend shut down trap catches. These results indicate that the pheromone blend consists of 3Z,6Z,9Z-21:H and 3Z,9Z-6S,7R-epoxy-21:H. This is the first report of a hydrocarbon/epoxide pheromone for a prey species of this bolas spider. Sex attractants or pheromones for the other three prey species are composed of aldehydes or acetates.