Economics of spider orb-webs: the benefits of producing adhesive capture thread and of recycling silk

1. The replacement of dry, fuzzy cribellar prey capture thread by viscous, adhesive capture thread was a major event in the evolution of orb-weaving spiders. Over 95% of all orb-weaving species now produce adhesive threads.
2. Adhesive thread achieves its stickiness with a much greater material economy than does cribellar thread.
3. Transformational analyses show that, relative to spider mass, adhesive orb-weavers invest less material per mm of capture thread and produce stickier capture threads than do cribellate orb-weavers.
4. The total cost of producing an orb-web that contains cribellar thread is reduced by 32% when a spider recycles its silk and another 34% when these capture threads are replaced by adhesive threads of equal stickiness.
5. The increased economy with which adhesive capture thread achieves its stickiness may have been an important factor that favoured the origin and success of modern orb-weaving spiders that produce adhesive capture threads.     

Capture thread extensibility of orb-weaving spiders: testing punctuated and associative explanations of character evolution

Spider orb-webs contain sticky prey capture threads and non-sticky support threads. Primitive orb-weavers of the Deinopoidea produce dry cribellar threads made of thousands of silk fibrils that surround supporting axial fibres, whereas the viscous threads of modern Araneoidea orb-weavers produce adhesive threads with an aqueous solution that coalesces as droplets around the axial fibres. We have previously shown that the greater diversity of the Araneoidea is phylogenetically significant and attributed this disparity to a number of advantages, considered key innovations, that adhesive thread has over cribellar thread. An important putative advantage of adhesive thread demonstrated by Kohler and Vollrath in their 1995 study is its greater extensibility, a feature that better adapts it to absorb the kinetic energy of a prey strike. However, this conclusion is based on a two-species comparison that does not take advantage of the modern comparative method that requires hypotheses to be tested in a phylogenetic context. Using a transformational analysis to examine threads produced by nine species, our study finds no support for the punctuated explanation that adhesive thread has a greater extensibility than cribellar thread. Instead, it strongly supports the associative null hypothesis that capture thread extensibility is tuned to spider mass and to architectural features of the web, including its capture area, capture spiral spacing, and capture area per radius.     

Changes in spinning anatomy and thread stickiness associated with the origin of orb-weaving spiders

The cribellum is an oval spinning field whose spigots produce silk fibrils that form the outer surfaces of the primitive prey capture threads found in aerial spider webs. A comparison of the cribella and cribellar capture threads of 13 species of spiders representing seven families (Amaurobiidae, Desidae, Dictynidae, Filistatidae, Neolanidae, Oecobiidae, and Uloboridae) confirms that the stickness of a cribellar thread is directly related to the number of spigots on a spider's cribellum. This comparison also demonstrates that the origin of orb-weaving spiders from ancestors that constructed less highly organized webs was associated with increases in both the weight-specific number of cribellum spigots and the weight-specific stickiness of cribellar prey capture threads. In contrast to other cribellate spiders, the number of cribellum spigots of orb-weaving species of the family Uloboridae scales to spider mass. Thus, the origin of orb-weaving spiders involved not only behavioural changes that stylized and restricted the placement of cribellar threads, but also included morphological changes that increased the stickiness of these capture threads by endowing them with more cribellar fibrils.     

Adhesive compatibility of cribellar and viscous prey capture threads and its implication for the evolution of orb-weaving spiders

Evolution of orb-weaving spiders that comprise the Orbiculariae clade involved a transition in the composition of prey capture thread that has been challenging to explain. The primitive cribellar threads spun by members of the Deinopoidea subclade resemble the capture threads of their non-orb-web-weaving ancestors and are formed of thousands of fine, dry, protein cribellar fibrils. In contrast, the derived viscous capture threads spun by members of the Araneoidea subclade have regularly spaced, aqueous adhesive droplets. When second instar deinopoid spiderlings emerge from egg sacs they are unable to spin cribellar threads, and, therefore, do not construct orb-webs; whereas second instar araneoids spin capture threads and construct orb-webs. If, as we hypothesize, viscous material evolved to enable second instar spiderlings to construct orb-webs, early araneoids may have spun composite cribellar-viscous capture threads. To examine the functional feasibility of such intermediate capture threads, we compared the adhesion of cribellar threads, viscous threads, and combined cribellar-viscous threads. The stickiness of these combined threads was greater than that of native cribellar or viscous threads alone. The viscous material of Araneus marmoreus threads exhibited a substantial increase in stickiness when combined with cribellar fibrils and that of Argiope aurantia threads a small increase in stickiness when combined with cribellar fibrils. Thus, if early araneoids retained their ability to spin cribellar threads after having evolved glands that produced viscous material, their composite threads could have formed a functional adhesive system that achieved its stickiness at no loss of material economy.     

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.     

Adhesive efficiency of spider prey capture threads

Cribellar capture threads are comprised of thousands of fine silk fibrils that are produced by the spigots of a spider's cribellum spinning plate and are supported by larger interior axial fibers. This study examined factors that constrain the stickiness of cribellar threads spun by members of the orb-weaving family Uloboridae in the Deinopoidea clade and compared the material efficiency of these threads with that of viscous capture threads produced by members of their sister clade, the Araneoidea. An independent contrast analysis confirmed the direct relationship between cribellar spigot number and cribellar thread stickiness. A model based on this relationship showed that cribellar thread stickiness is achieved at a rapidly decreasing material efficiency, as measured in terms of stickiness per spigot. Another limitation of cribellar thread was documented when the threads of two uloborid species were measured with contact plates of four widths. Unlike that of viscous threads, the stickiness of cribellar threads did not increase as plate width increased, indicating that only narrow bands along the edges of thread contact contributed to their stickiness. As thread volume increased, the gross material efficiency of cribellar threads decreased much more rapidly than that of viscous threads. However, cribellar threads achieved their stickiness at a much greater gross material efficiency than did viscous threads, making it more challenging to explain the transition from deinopoid to araneoid orb-webs.     

The effects of capture spiral composition and orb-web orientation on prey interception

Cribellar prey capture threads found in primitive, horizontal orb-webs reflect more light, including ultraviolet wavelengths, than viscous threads found in more derived, vertical orb-webs. Low web visibility and vertical orientation are each thought to increase prey interception and may represent key innovations that contributed to the greater diversity of modern, araneoid orb-weaving spiders. This study compares prey interception rates of cribellate orb-webs constructed by Uloborus glomosus (Uloboridae) with viscous orb-webs constructed by Leucauge venusta (Tetragnathidae) and Micrathena gracilis (Araneidae). We placed sectors of cribellar and viscous threads side by side in frames that were oriented either horizontally or vertically. The webs of both U. glomosus and L. venusta intercepted more prey when vertically oriented. In each orientation L. venusta webs intercepted more insects than did U. glomosus. Although this is consistent with the greater visibility of cribellar threads, the more closely spaced capture spirals of L. venusta may have contributed to this difference. Micrathena gracilis webs intercepted more prey than did U. glomosus webs, although web orientation did not affect the performance of this araneoid species. The stickier and more closely spaced capture spirals of M. gracilis may have enhanced the interception rates of this species and accounted for the greater number of smaller dipterans retained in its webs. The tendency for these slow, weak flight insects to be blown into both horizontal and vertical webs may account for similar interception rates of horizontal and vertical M. gracilis webs. These observations support the enhanced prey interception of vertically oriented orb-webs, but offer only qualified support for the contributions of lower visibility viscous capture threads.     

Persistent stickiness of viscous capture threads produced by araneoid orb-weaving spiders

The most commonly encountered spider orb-webs rely on sticky, viscous capture threads to retain prey. These threads are composed of supporting fibers covered by a complex aqueous solution that forms a series of droplets, each with a glycoprotein granule that confers adhesion. This adhesive system normally functions for less than a day before being replaced. Despite their ephemeral nature, we found that the stickiness of viscous threads persists for much longer. When measured over the course of 7 days, small decreases in the adhesion of Larinioides cornutus threads were not statistically significant. Threads of Araneus marmoreus, Argiope trifasciata, and Metepeira labyrinthea were aged for 8-10 months and remeasured under environmental conditions similar to those under which initial measurements were made. When returned to humidity similar to that under which measurements were initially made, neither the droplet volumes nor the stickiness of aged threads differed significantly from those of newly spun threads. These observations indicate that when viscous threads are protected from contamination, the compounds responsible for their hydrophilic and adhesive properties do not degrade easily.     

Evolution of adhesive mechanisms in cribellar spider prey capture thread: evidence for van der Waals and hygroscopic forces

Sticky prey capture threads are produced by many members of the spider infraorder Araneomorphae. Cribellar threads are plesiomorphic for this clade, and viscous threads are apomorphic. The outer surface of cribellar thread is formed of thousands of fine, looped fibrils. Basal araneomorphs produce non-noded cribellar fibrils, whereas more derived members produce noded fibrils. Cribellar fibrils snag and hold rough surfaces, but other forces are required to explain their adherence to smooth surfaces. Threads of Hypochilus pococki (Hypochilidae) formed of non-noded fibrils held to a smooth plastic surface with the same force under low and high humidities. In contrast, threads of Hyptiotes cavatus and Uloborus glomosus (Uloboridae) formed of noded fibrils held with greater force to the same surface at intermediate and high humidities. This supports the hypothesis that van der Waals forces allow non-noded cribellar fibrils to adhere to smooth surfaces, whereas noded fibrils, owing to the hydrophilic properties of their nodes, add hygroscopic forces at intermediate and high humidities. Thus, there appear to have been two major events in the evolution of adhesive mechanisms in spider prey capture thread: the addition of hydrophilic nodes to the fibrils of cribellar threads and the replacement of cribellar fibrils by viscous material and glycoprotein glue.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 1–8.     

Factors governing the stickiness of cribellar prey capture threads in the spider family Uloboridae

The surface of a cribellar prey capture thread is formed of thousands of fine, looped fibrils, each issuing from one of the spigots on an oval spinning plate termed the cribellum. This plesiomorphic capture thread is retained by members of the family Uloboridae, in which its stickiness differs among genera. An examination of five cribellar thread features in nine uloborid species shows that only the number of fibrils that form a thread explains these differences in thread stickiness. Neither the physical features of these fibrils, nor the manner in which they are combined to form threads differs among species. Threads produced by orb-weaving species contain fewer fibrils than those produced by species that build reduced webs. Relative to spider weight, the number of fibrils that form a cribellar thread is greatest in simple-web species of the genus Miagrammopes, less in triangle-web species of the genus Hyptiotes, and least in orb-weaving species representing five genera. A transformational analysis shows that change in the number of cribellum spigots is directly related to change in the stickiness of cribellar thread. This direct relationship between the material invested in a cribellar thread and its stickiness may have been a limiting factor that favored the switch from the dry cribellar threads of uloborids to the adhesive capture threads produced by other orb-weaving families. © 1994 Wiley-Liss, Inc.     

Functional organization of the spinning apparatus of Cyrtophora citricola with regard to the evolution of the web (Araneae,Araneidae)

Summary The spinning apparatus of Cyrtophora citricola closely corresponds to that of orb-weaving Araneidae, two peculiarities excepted. Firstly the spigots of the piriform glands differ extremely in size, the smallest of them being numerous and having a unique location on the anterior spinnerets. Secondly, the triad complex (on the posterior spinnerets) used by other Araneidae for producing gluey capture threads is lacking. Both these characteristics are correlated with the construction of a fine meshed sheet of dry silk by Cyrtophora instead of orbwebs with capture spirals. The sheet can be understood as being a very much enlarged central area of orb-webs. Since vestiges of triads could be found in early developmental stages of C. citricola, the origin of the meshed sheet from orb-webs with gluey capture threads is clearly demonstrated. The paper includes a study on how the spider produces thread attachments by means of the secretions of the piriform glands.     

Spiders spinning electrically charged nano-fibres

Most spider threads are on the micrometre and sub-micrometre scale. Yet, there are some spiders that spin true nano-scale fibres such as the cribellate orb spider, Uloborus plumipes. Here, we analyse the highly specialized capture silk-spinning system of this spider and compare it with the silk extrusion systems of the more standard spider dragline threads. The cribellar silk extrusion system consists of tiny, morphologically basic glands each terminating through exceptionally long and narrow ducts in uniquely shaped silk outlets. Depending on spider size, hundreds to thousands of these outlet spigots cover the cribellum, a phylogenetically ancient spinning plate. We present details on the unique functional design of the cribellate gland–duct–spigot system and discuss design requirements for its specialist fibrils. The spinning of fibres on the nano-scale seems to have been facilitated by the evolution of a highly specialist way of direct spinning, which differs from the aqua-melt silk extrusion set-up more typical for other spiders.     

Microstructural Analysis of the Capture Thread Spinning Apparatus in Orb Web Spiders

The microstructural characteristics of the capture thread production from silk glands in the orb web spiders were analyzed using scanning and transmission electron microscopes. Sticky and gluey capture threads of the web are originated from the silks of two flagelliform glands and four aggregate glands. They supply precursors of the secretory silks to a pair of characteristic “triad” spinning units on the posterior spinnerets. The aggregate gland is composed of large and multi‐lobed secretory region and thick excretory duct surrounded by large irregular nodules. The excretory duct of this gland basically consists of three superposed types of cells which are inner columnar epithelium, nodule forming cells and outer connectives. The nodules contain numerous mitochondria and glycogen particles within their cytoplasm and they are surrounded by the same sheath of thin connective tissues. Secretory region of the aggregate gland which produce water‐soluble components of the capture thread comprises discrete secretory vesicles and extensive rough endoplasmic reticulum. Characteristically, secretory droplets are formed without involvement of the Golgi complexes, suggesting that they do not play an important role in the processing of the capture threads. However the electron densities and internal textures of the granules are observed with diverse according to their maturation level. Finally, the secretory products are released by the mechanism of apocrine secretion losing part of their cytoplasm during this process.     

Fine structural analysis on triad spinning spigots of an orb‐web spider's capture threads

Capture threads of the golden orb‐web spider Nephila clavata are produced from the silks of a pair of triad spinning units composed of a flagelliform gland (FLG) and two aggregate glands (AGG). In N. clavata, arrangement of the triad spigots is closely related to coating an axial supporting fiber with sticky aqueous droplets on a continuous and consistent basis for capture thread production. The central spigot of FLG and peripherally located AGG spigots are aligned along a single plane, and both have bullet‐type spigots with flexible segments. In particular, the pear‐shaped spigot of the AGG with a wide‐aperture nozzle provides not only sufficient luminal space for controlling transient storage of the aqueous gluey substance but also an effective spatial system that thoroughly coats the axial fibers with a viscous aqueous solution.     

Evolution beyond the orb web: the web of the araneid spider Pasilobus sp., its structure, operation and construction

The araneid spider Pasilobus sp., common in the Morobe District, New Guinea, builds its web at night close to bushes and small trees. The more-or-less horizontal web has a triangular frame that is divided into halves by a midline thread running from the apical angle to bisect the base. From the midline thread hang 4–11 pairs of widely spaced spanning threads; these are the only adhesive elements in the web. The spanning threads are viscid for only part of their length and are strongly attached to the web only at their junction with the midline thread. The outer end of each spanning thread forms an easily ruptured, low-shear joint with the lateral frame thread of the web. When a flying insect strikes a spanning thread, the low-shear joint breaks and the thread drops below the web, leaving the insect tethered to the midline. The insect may continue to fly, on the tether, or may spin down to motionlessness. The spider rushes to the midline thread end of the tether, hauls up the spanning thread and then bites the insect. Experimental investigations of the low-shear joints and the adhesiveness and elasticity of the spanning thread are described and the results analysed. The web-building behaviour of Palilobus differs in several ways from that of most araneids and is described and compared with that of Gasteracantha and other species. The possible evolutionary origins of the Pasilobus web are outlined.     

More data, fewer shifts: molecular insights into the evolution of the spinning apparatus in non-orb-weaving spiders

All spiders produce silk and use it for various functions throughout their lives, but not all spiders produce the same silks, or use them for the same functions. These functions may include building shelters, protecting eggs, and trapping prey. The "RTA clade" of spiders (grass spiders, jumping-spiders, wolf spiders, hackled-band weavers, etc.) is an extremely diverse group ( approximately 18,000 species, representing nearly half of all described species), with great variation in ecology and morphology, including variation in the cribellum, a specialized silk-producing organ. The loss of the cribellum, a structure that produces fibers contributing stickiness to prey snares and which is invariably associated with a set of accessory structures, has been studied in orb-web-weavers and shown to have been lost once during the evolutionary history of the group, but never regained. Relative to the orb-weavers, evolution of the structure remains less-thoroughly studied in the RTA clade. As the cribellum is one member of a suite of traits, the combined action of which is essential in prey-capture, its loss should have ecological correlates or physiological trade-offs of evolutionary interest. Using molecular data from nuclear genes (ribosomal DNAs 18S and 28S, and protein-coding Histone H3), as well as mitochondrial data (Cytochrome oxidase I) totaling approximately 3400 base pairs, we developed a phylogenetic hypothesis for three-clawed lineages in this group, focusing on families where taxonomy and previous cladistic analyses suggest multiple losses, or possibly loss and secondary gain, of the cribellum. Results of Bayesian and direct-optimization (POY) analyses agree on a well-resolved and robust agelenid clade that includes the putative subfamilies Ageleninae, Tegenariinae, Textricinae and Coelotinae, but excludes the cribellate New Zealand genus Neoramia. Optimizing the pattern of cribellum evolution onto these trees shows that the cribellate state is conserved in large clades and has undergone fewer shifts than current taxonomy implies. The dominant pattern is one of repeated loss of the cribellum, though loss and regain remains a possibility in some groups.     

Untangling the Tangle-Web: Web Construction Behavior of the Comb-Footed Spider Steatoda triangulosa and Comments on Phylogenetic Implications (Araneae: Theridiidae)

Theridiidae typically construct a three-dimensional web often described as irregular. The web consists of a supporting structure and lines under tension termed gumfooted lines. We used automated methods to observe web construction in the theridiid Steatoda triangulosa under laboratory conditions. Web construction lasted several nights. After orientation, spiders built a three-dimensional structure of several threads radiating sideways and downward from the retreat. To build gumfooted lines, they started from the retreat, moved along a structural thread, then dropped down to attach the thread to the lower substrate. On returning, they coated the lowest part of the thread with viscid silk before moving up along the same thread back to the structural thread. They then continued moving along the same structural thread to drop down again to build the next gumfooted line. This behavior was continued until the spiders had built a series of gumfooted lines (a bout). There were regular intervals between the construction of two bouts. Thus, a single web included many bouts built in different stages. We show that gumfooted lines are not homologues to sticky web elements of orb-weavers and present new synapomorphic characters that support the monophyly of Theridiidae + Nesticidae and the monophyly of araneoid sheet web weavers. Further, the time allocation pattern for different behavioral stages and the fine structure of a gumfooted line are presented.     

Evolution of aerial spider webs coincided with repeated structural optimization of silk anchorages

Physical structures built by animals challenge our understanding of biological processes and inspire the development of smart materials and green architecture. It is thus indispensable to understand the drivers, constraints, and dynamics that lead to the emergence and modification of building behavior. Here, we demonstrate that spider web diversification repeatedly followed strikingly similar evolutionary trajectories, guided by physical constraints. We found that the evolution of suspended webs that intercept flying prey coincided with small changes in silk anchoring behavior with considerable effects on the robustness of web attachment. The use of nanofiber based capture threads (cribellate silk) conflicts with the behavioral enhancement of web attachment, and the repeated loss of this trait was frequently followed by physical improvements of web anchor structure. These findings suggest that the evolution of building behavior may be constrained by major physical traits limiting its role in rapid adaptation to a changing environment.     

Biomechanical variation of silk links spinning plasticity to spider web function

Spider silk is renowned for its high tensile strength, extensibility and toughness. However, the variability of these material properties has largely been ignored, especially at the intra-specific level. Yet, this variation could help us understand the function of spider webs. It may also point to the mechanisms used by spiders to control their silk production, which could be exploited to expand the potential range of applications for silk. In this study, we focus on variation of silk properties within different regions of cobwebs spun by the common house spider, Achaearanea tepidariorum. The cobweb is composed of supporting threads that function to maintain the web shape and hold spiders and prey, and of sticky gumfooted threads that adhere to insects during prey capture. Overall, structural properties, especially thread diameter, are more variable than intrinsic material properties, which may reflect past directional selection on certain silk performance. Supporting threads are thicker and able to bear higher loads, both before deforming permanently and before breaking, compared with sticky gumfooted threads. This may facilitate the function of supporting threads through sustained periods of time. In contrast, sticky gumfooted threads are more elastic, which may reduce the forces that prey apply to webs and allow them to contact multiple sticky capture threads. Therefore, our study suggests that spiders actively modify silk material properties during spinning in ways that enhance web function.