Web building strategies in Araneids and their kin
From the enormous silken palaces of social spiders to the single line of the bola spider, webs form an integral part of our perception of spiders. However, these silken structures occur in such a bewildering array of form and function that they often defy simple classification and are often more complicated than they may at first appear.
When asked to name a typical spider, most people point to the Araneids (orbweavers), unaware of how highly derived the ability to construct webs really is. Primitive spiders such as the mygalomorphs produce silk to line their burrows and to wrap their prey; however it is only ~300 million years later with the evolution of araneomorphs and the co-evolution of flying insects that silk has taken on a primary role in prey capture. Even within the araneomorphs, web building strategies have evolved in distinct steps echoing the evolution of their prey. 380 million years ago (MYA) Attercopus fimbriungus (Mesothelidae) shared its environment with hexapods, those most primitive of insects. 250 MYA, insects have radiated widely, among them are the flying insects, meanwhile spiders have also evolved to encompass the mygalomorphs, which have undergone a physiological rearrangement of their spinnerets from the middle of their abdomens to the rear; a change thought to be important in the development of more elaborate webs. By ~200MYA the first araneomorphs appeared in the form of the Filistatidae, the most primitive web builders whose web consists of nothing more than tubular webbed retreat with several triplines to alert the spider to the presence of prey. However this innovative use of silk resulted in an explosive radiation of species so that 90% of spiders today fall into the araneomorphs. Subsequent development of the triplines into an actual trap developed in the Eresidae. These webs however were still confined to the ground. Hence, the next step was to take advantage of the large, untapped supply of prey in the form of flying insects. This required abandoning the safety provided by their ground dwellings and moving into a less protected aerial environment. The Dictynidae were the earliest colonizers of this new niche and formed the first silken structures readily identified as webs. They didn’t immediately start spinning in the treetops, but rather spun their webs close to the ground between low lying plants. Their webs made of cribellate silk are a haphazard array of silken strands with no apparent order. Movement into the higher reaches was hampered by several problems, including the expense of producing silk, the change in prey type and the greater consideration to aerodynamics. These considerations required a different technique to web building, one which resulted in a more organized framework resulting in a definitive centre and supporting radii. This problem was solved by Sybota sp.. From this point, only relatively minor changes were required to construct the archetypal centric design with central hub and radii commonly recognized in orbweavers and uloboridae.
The evolution of web design would not be possible without the co-evolution of its building blocks, silk. Modern araneomorphs have up to 7 types of silk produced from 3-5 different spinnerets, however, despite the marked differences in their physical properties, these differences can be primarily traced to the spidroin protein which composes 90% of the silk. Separate spidroin molecules share a remarkable similarity in codon sequence, number and length indicating a common evolutionary heritage, unsurprising considering its composition; ~42% glycine and ~24% alanine. Such highly repetitive sequences make for evolutionary hotspots, especially by frameshift and duplication mutations.
A greater appreciation of unusual web building practices can be had by first observing the common orb weavers. First a main line is erected by drifting a strand of silk across a gap. Once this line contacts a suitable anchor point, it is reinforced until it can support the entire web. Given the high tensile strength of silk this typically requires only a few threads. From this line a loose loop is hung which is then tightened into a ‘Y’ shape by pulling it taught with a secondary thread connected at the loop’s centre and pulled downward. This intersection will be the centre of the proto-hub or web epicentre, from which will originate the proto-radii. Proto-radii or anchor lines are constructed by walking along one of the original ‘Y’ strands and either walking down to another connection point, or dangling with a dragline. The ‘Y’ has now become more of a star shape and can now be framed by a roughly rectangular box which acts as a framework to attach the radii of the web. A bridge thread is the first line in the frame and is the highest line in the web. Consider the frame like the rim of a wheel and the radii as the spokes. After the radii are constructed, a ring of concentric circles originating at the centre and expanding towards the frame is deposited. Up to this point, only non-sticky (major-ampullate) silk has been used as these radii are what the spider uses to move around the web. Spider silk is essentially a liquid crystalline solution consisting of a crystallized poly-alanine/glycine Beta sheet fraction [with differential orientation, strength and size (depending on amino acid composition)] within an amorphous matrix of glycine biased composition (alanine/glycine have small side groups allowing tighter packing). This solution forms an organized thread as the dope in the silk gland passes along a canal in which the pH drops from 7 to 6 resulting in uncoiling of the spidroin molecules. The narrowing canal of the spinnerets aligns the hydrophobic poly-alanine regions into Beta pleated sheets which exclude water. As dope is pulled from the silk gland the mechanical stretch further excludes water resulting in coagulation and hardening of the solution into a solid state. The properties of the silk varying with the amount of stretch applied, the type of silk, the species of spider, etc…
Now the spider is ready to deposit the sticky (capture) silk, retracing the path it just took, it lays the capture silk as it consumes the non-sticky silk until it arrives at the hub where it sits and waits. Differences between major-ampullate and capture silk are reflected in a larger and smaller fraction of the crystallized moiety, respectively. The former being more rigid and the latter more flexible. Capture silk is composed of an especially sticky, flexible silken axial core strand produced by 1 spinneret and interspersed with globules of glycoprotein produced concurrently by 2 other spinnerets. The silk owes its increase in volume and stickiness to absorption/adsorption of water molecules (by hydrophilic pyrrolidines) from the surrounding environment (hygroscopy), resulting in physical alteration of the silk due to incorporation of the water. These pyrrolidines, composed of proline, also break up the stacked hydrophobic poly-alanine/glycine beta sheet organization (providing rigid strength) of the silk, introducing flexibility. However, the spider faces a conundrum; its web must be able to trap both low and high velocity insects. The solution is as complicated as it is elegant and is solved by having essentially two silks in one, or a silk which changes physical properties with increased extension. Capture silk is formed by a tight coil of polymeric threads connected by a network of molecular springs arranged in series and in parallel. At low extension (low velocity insect), the tight coil extends into long chain with a linear increase in tensile strength resulting from the springs arranged in series and held by a cooperation of 3-4 hydrogen (H) bonds/Beta sheet and Van der Waals forces (VDW). As an increasing degree of stress is applied (high velocity insect), extension increases, the H and VDWs bonds break and the springs arranged in parallel take over, resulting in an exponential increase in tensile force. H and VDWs bonds are dubbed sacrificial bonds since unlike metallic, ionic or covalent bonds, they are able to reform, as the springs relax, resulting in a kind of bio-healing material which can return to its original structural properties. Furthermore, the glycoprotein globules consisting of a viscous, aqueous salt coat behave as a viscoelastic solid, such that at low extensions the adhesion forces increase linearly (like a normal spring) however at high extensions (high impact, fast flying insect), the adhesion forces increase exponentially due to high viscous effects. As though this process is not complicated enough, many spiders have diverted from this plan, opting for their own unique methods.
The first araneomorphs to employ silk as a capture method used cribellate silk, an elaborate structure composed of an axial core of paired pseudoflagelliform silk strands, progenitor to the capture silk of araneids, which act as a scaffold for the actual capture threads, cribellate silk. This silk does not employ glue, in fact the webs are completely dry such that placed in an arid environment the web retains its ability to capture prey almost indefinitely (supposing it is not subject to particulates). Rather, the capture threads entangle their prey. When one invests some thought into this problem, this concept is actually quite non-intuitive and difficult to understand without a detailed examination of the microscopic structure. How does a web built in a flat plane capture and hold its prey without the sticky capillary forces of liquids? Furthermore, an insect’s incredibly hard exoskeleton is composed of chitin (embedded in a proteinaceous matrix), a modified polysaccharide often shaped into smooth, flat or rounded lines, geometries extremely difficult to hold onto, especially when the insect is struggling to free itself. Like the seed of the burdock (burr) which fastens to the loops in objects by means of tiny hooks, cribellum silk takes this concept and reduces it to the nanoscale 10^-9 metres); cribellar silk (loops) bind to the prey surface (hooks) by means of innumerable VDWs bonds and hygroscopic forces. Additionally, the flexibility of the silken strands increases the surface area of contact while dissipating the stress along the longitudinal plane. Cribellar threads are not extruded from the spinnerets like other silk, but rather are produced in an anterior plate called the cribellum. This plate is formed from a dense array of spigots (40-60,000), each one producing a cribellar thread as thin as 10-100nm in diameter. These are then hackled in a laborious process achieved through comb-like appendages on the meta-tarsi of cribellate spiders, the calamistrum. It is this hackling which charges the cribellate fibrils, causing them to repel one another and expand into a disorganized, entangling matrix of characteristic wooly appearance.
The concept of organisms working towards greater complexity through evolution is a great misconception, one which is well illustrated by a comparison between viscid silk in the Araneids and cribellate silk of their ancestors. The idea of increased complexity is supported by the modular design of many biological systems, each innovation built on the previous one until it reaches the purported pinnacle of the present day. However, biological systems respond only to environmental pressures. Thus any system which can minimize its energy expenditure while enabling the propagation of its genes has a selective advantage. Thus all other considerations being equal, a different biological system has an equal likelihood of being adopted and propagated within a population and a simpler biological system has a greater likelihood of being adopted over a complex one if it leads to the aforementioned advantages. The latter consideration has a greater probability during early development of a trait when its inherent advantage is smaller or else during environmentally dynamic periods. 95% of araneomorphs fall within the araneids, employing viscid silk. How then was the complex cribellate silk superseded by viscid silk? Capture thread was once thought to offer greater extensibility, enabling the capture of a greater diversity of prey. Recent studies have shown however that despite the greater extensibility of capture silk relative to the pseudoflagelliform silk forming the axial core, the cribellar threads increase the range of extensibility (up to 500%) so that a web may maintain its structural integrity after the rupture of the core strands. Unlike capture silk it also fails gradually, as different groups of nanofibres succeedingly fail (unlike capture silk which fails suddenly). In fact, more than 90% of energy absorption occurs after core failure. The answer to Araneid dominance appears to lie in the rise of a key innovation, glue, which drastically reduces that energetic expenditure. However it is the very complexity of cribellate silk, requiring a large investment of energy and time that makes such a viable alternative.Thus it is how extensibility and stickiness is achieved, rather than the degree of extensibility. Moreover, major ampullate (flagelliform) silk is not only tougher than pseudoflagelliform silk, but also capable of handling greater stress, enabling its use in supplementary applications. The rapidity with which it can be extruded, coincident with glycoprotein globule incorporation, offers an advantage especially in ecological niches where web destruction is prevalent. Other factors like decreased UV reflectance are also thought to have played a role.
Subterfuge is the name of the game within the Cyclosa genus. Recognized by their elongated abdomens, these spiders after completing the basic web outlined above incorporate detritus and insect remains into their webs along either discoid or axial stabilimenta (a white, opaque silk). The purpose of this brand of silk remains contested, though studies have shown that prey capture rates may increase by as much as 50%. This intriguing phenomena is likely due to the silk’s reflectance properties, which extends across the entire insect spectral range including UV, an adaptation to UV-vision biased insects. Stabilimenta also increases the size of the spider sometimes by as much as 10x and since nature is governed by the general principle that size and strength are correlated, this form of mimicry may decrease their desirability to predators such as wasps. Other theories include alerting avifauna and other large bodied animals to the presence of the web or else, as the name would suggest, to stabilize the web, since stabilimentum silk has a greater strength and crystalline structure than either capture or dragline silk used in the rest of the web. Stabilimentum often has detritus and insect remains woven into it helping to serve as camouflage and perhaps even as a chemoattractant in the form of pheromones, in addition to the aforementioned properties. Interestingly this controversial topic neglects to take into account the various patterns employed by different araneids in their use of stabilimentum silk. Even within a genus (eg. Argiope) different species produce different patterns which may even change in response to ecological factors. Studies have shown that spiders change from linear to helical stabilimentum in response to several factors; in windy conditions some spiders will incorporate a greater amount of helical stabilimentum to strengthen the web and reduce flexibility which might otherwise negatively impact a spider’s ability to differentiate oscillations caused by prey from those caused by the wind. A second interesting behavioural adaptation is in response to hunger. Helical stabilimentum results in an increased tension on the lines which in turn increases the amplitude of vibration so that smaller prey, normally ignored by a well sated spider, can be detected and eaten.
- Cyclosa insulana with elaborate, spiral stabilimentum.
- Cyclosa sp. with web debris arranged to camouflage itself
- Cyclosa with another camouflaging design.
In a curious quirk of evolution, the Deinopidae or net casting spiders which branched early on from the araneids combine web building with a more active hunting strategy. They build a small rectangular web, stretch it between their front two pairs of legs and dangling motionlessly above their prey, ambush them. Unlike in araneids, the capture silk is replaced with cribellate silk (which gives it a wooly appearance), however it remains just as efficient at trapping prey. Deinopid webs remain similar to the aforementioned orbweaver template with several variations important for prey capture. Dangling as it does, how does a deinopid drop fast enough to ensnare its prey? The answer lies in two modifications to web design. First, a vertical safety thread tethers the web and gives it a slight conical shape while construction is in progress. When the web is completed, the spider holds this high tension safety thread with its second pair of hind legs. When prey passes by, it releases the safety line catapulting the spider forward at great speed. Another difference is the use of a bridge line, built slightly above the capture web. This line is held with with the first pair of hind legs and allows the spider a surface to pull down on to generate a downward force.
- Deinopis spider with net.
Hanging pendulously from her perch, she remains still, her camouflaged form allowing her to blend in seamlessly with the branches overhead. She waits until nightfall when her huge anterior median eyes provide an unrivalled night vision, their lenses with an f/0.58 (f=aperture size, smaller number being large diameter) mean they are able to concentrate light more efficiently than a cat (f/0.9) or an owl (f/1.1). She owes this sensitivity to the light activated molecule rhodopsin, tightly packed into a microvillar membrane (which dramatically increases the surface area). Amazingly, 1500 times as many photons reach the light receptors in her eyes than the rods in our own eyes. She even accomplished this without the presence of a tapetum, a reflective membrane used to concentrate available light in many other nocturnal animals. Her preparation is impressive, she has staked out an ambush location, first having inspected it for loose debris and anything that might entangle her web, next she builds her web tentatively prodding the ground with her foot, ensuring it is set at the proper height. She may have even gone so far as to drop several faecal spots to guide her aim. In this manner she hangs, and patiently waits … An insect passes below, oblivious to the danger above. In a fraction of a second, the safety line has been cut, the web has been stretched 4 times its former size and before the insect even recognizes the danger, it finds itself helplessly trapped, venom coursing through its body. She feeds. However her work is not done. The rhodopsin which enables her unparalleled night vision is so sensitive to light that daytime exposure would actually destroy it. Thus, at dawn, the spider spends the first 2 hours dismantling the light sensitive microvillar membrane and rhodopsin molecules. The latter subsequently migrate behind a protective pigment layer, effectively rendering them less sensitive to light. When dusk falls, the light sensitive membrane is once again renewed, web building is resumed and the hunt can begin anew.
With a single silken line, four eyes and no venom, Miagrammopes spp. within the Uloboridae family hardly seem to meet the definition of a spider at all. However one would be remiss to underestimate these diminutive spiders. Cryptically coloured, they weave a single resting thread of dragline silk to which they attach two or more strands of cribellate capture silk. Then they pull the web under tension, holding the slack in a loop under their bodies. When prey approaches, they release the tension and let the web entangle the prey. Once caught, a series of progressive jerks further entangles the prey. Once the spider is satisfied, it will apply cribellate silk to ensure the insect’s incapacitation. Next they proceed to wrap their prey in copious amounts of silk; up to 74 minutes of wrapping, producing 80m of silk has been recorded for a single prey item. Recent studies suggest that this wrapping strategy, which exceeds the time spent by orbweavers by several orders of magnitude, constitutes an important adaptation for subduing prey in this venom-less family. Through the summation of small tensions on the sticky lines, sufficient compressive force is generated to break legs or even kill prey. Additional force may develop by way of supercontraction, a phenomenon by which silk shrinks 50% of its original length through changes in water content. Despite these incredible insights into this genus’ behaviour, the simple question of how a single line proves effective at catching prey remains a mystery.
- Miagrammopes sp.
- Miagrammopes sp. with prey.