Behavioural and biomaterial coevolution in spider orb webs

Mechanical performance of biological structures, such as tendons, byssal threads, muscles, and spider webs, is determined by a complex interplay between material quality (intrinsic material properties, larger scale morphology) and proximate behaviour. Spider orb webs are a system in which fibrous biomaterials—silks—are arranged in a complex design resulting from stereotypical behavioural patterns, to produce effective energy absorbing traps for flying prey. Orb webs show an impressive range of designs, some effective at capturing tiny insects such as midges, others that can occasionally stop even small birds. Here, we test whether material quality and behaviour (web design) co‐evolve to fine‐tune web function. We quantify the intrinsic material properties of the sticky capture silk and radial support threads, as well as their architectural arrangement in webs, across diverse species of orb‐weaving spiders to estimate the maximum potential performance of orb webs as energy absorbing traps. We find a dominant pattern of material and behavioural coevolution where evolutionary shifts to larger body sizes, a common result of fecundity selection in spiders, is repeatedly accompanied by improved web performance because of changes in both silk material and web spinning behaviours. Large spiders produce silk with improved material properties, and also use more silk, to make webs with superior stopping potential. After controlling for spider size, spiders spinning higher quality silk used it more sparsely in webs. This implies that improvements in silk quality enable ‘sparser’ architectural designs, or alternatively that spiders spinning lower quality silk compensate architecturally for the inferior material quality of their silk. In summary, spider silk material properties are fine‐tuned to the architectures of webs across millions of years of diversification, a coevolutionary pattern not yet clearly demonstrated for other important biomaterials such as tendon, mollusc byssal threads, and keratin.     

The ecological and evolutionary interdependence between web architecture and web silk spun by orb web weaving spiders

Spider orb webs are dynamic, energy absorbing nets whose ability to intercept prey is dependent on both the mechnical properties of web design and the material properties of web silks. Variation in web designs reflects variation in spider web spinning behaviours and variation in web silks reflects variation in spider metabolic processes. Therefore, natural selection may affect web function (or prey capture) through two independent and alternative pathways. In this paper, I examine the ways in which architectural and material properties, singly and in concert, influence the ability of webs to absorb insect impact energy. These findings are evaluated in the context of the evolution of diverse aerial webs. Orb webs range along a continuum from high to low energy absorbing. No single feature of web architecture characterizes the amount of energy webs can absorb, but suites of characters indicate web function. In general, webs that intercept heavy and fast flying prey (high energy absorbing webs) are large, built by large spiders, suspended under high tension and characterized by a ratio of radii to spiral turns per web greater than one. In contrast, webs that intercept light and slow flying prey (low energy absorbing webs) are suspended under low tension, are small and are characterized by radial to spiral turn ratios that are less than one. The data suggest that for spiders building high energy absorbing webs, the orb architecture contributes much to web energy absorption. In contrast, for spiders that build low energy absorbing webs, orb architecture contributes little to enhance web energy absorption. Small or slow flying insects can be intercepted by web silks regardless of web design. Although there exists variation in the material properties of silk collected from high and low energy absorbing webs, only the diameter of web fibres varies predictably with silk energy absorption. Web fibre diameter and hence the amount of energy absorbed by web silks is an isometric function of spider size. The significance of these results lies in the apparent absence of selective advantage of orb architecture to low energy absorbing webs and the evolutionary trend to small spiders that build them. Where high energy absorption is not an exacting feature of web design, web architecture should not be tightly constrained to the orb. Assuming the primitive araneoid web design is the orb web, I propose that the evolution of alternative web building behaviours is a consequence of the general, phyletic trend to small size among araneoids. Araneoids that build webs of other than orb designs are able to use new habitats and resources not available to their ancestors.     

Functionally independent components of prey capture are architecturally constrained in spider orb webs

Evolutionary conflict in trait performance under different ecological contexts is common, but may also arise from functional coupling between traits operating within the same context. Orb webs first intercept and then retain insects long enough to be attacked by spiders. Improving either function increases prey capture and they are largely determined by different aspects of web architecture. We manipulated the mesh width of orbs to investigate its effect, along with web size, on prey capture by spiders and found that they functioned independently. Probability of prey capture increased with web size but was not affected by mesh width. Conversely, spiders on narrow-meshed webs were almost three times more likely to capture energetically profitable large insects, which demand greater prey retention. Yet, the two functions are still constrained during web spinning because increasing mesh width maximizes web size and hence interception, while retention is improved by decreasing mesh width because more silk adheres to insects. The architectural coupling between prey interception and retention has probably played a key role in both the macroevolution of orb web shape and the expression of plasticity in the spinning behaviours of spiders.     

A novel property of spider silk: chemical defence against ants

Spider webs are made of silk, the properties of which ensure remarkable efficiency at capturing prey. However, remaining on, or near, the web exposes the resident spiders to many potential predators, such as ants. Surprisingly, ants are rarely reported foraging on the webs of orb-weaving spiders, despite the formidable capacity of ants to subdue prey and repel enemies, the diversity and abundance of orb-web spiders, and the nutritional value of the web and resident spider. We explain this paradox by reporting a novel property of the silk produced by the orb-web spider Nephila antipodiana (Walckenaer). These spiders deposit on the silk a pyrrolidine alkaloid (2-pyrrolidinone) that provides protection from ant invasion. Furthermore, the ontogenetic change in the production of 2-pyrrolidinone suggests that this compound represents an adaptive response to the threat of natural enemies, rather than a simple by-product of silk synthesis: while 2-pyrrolidinone occurs on the silk threads produced by adult and large juvenile spiders, it is absent on threads produced by small juvenile spiders, whose threads are sufficiently thin to be inaccessible to ants.     

Does the Giant Wood Spider Nephila pilipes Respond to Prey Variation by Altering Web or Silk Properties?

Recent studies demonstrated that orb‐weaving spiders may alter web architectures, the amount of silk in webs, or the protein composition of silks in response to variation in amount or type of prey. In this study, we conducted food manipulations to examine three mechanisms by which orb‐weaving spiders may adjust the performance of webs to variation in prey by altering the architectures of webs, making structural changes to the diameters of silk threads, and manipulating the material properties or amino acid composition of silk fibers. We fed Nephila pilipes two different types of prey, crickets or flies, and then compared orb structure and the chemical and physical properties of major ampullate (MA) silk between groups. Prey type did not affect orb structures in N. pilipes, except for mesh size. However, MA silk diameter and the stiffness of orbs constructed by spiders fed crickets were significantly greater than for the fly group. MA fibers forcibly silked from N. pilipes fed crickets was significantly thicker, but less stiff, than silk from spiders fed flies. Spiders in the cricket treatment also produced MA silk with slightly, but statistically significantly, more serine than silk from spiders in the fly treatment. Percentages of other major amino acids (proline, glycine, and glutamine) did not differ between treatments. This study demonstrated that orb‐weaving spiders can simultaneously alter some structural and material properties of MA silk, as well as the physical characteristics of webs, in response to different types of prey.     

Developmental changes in barrier web structure under different levels of predation risk inNephila clavipes (Araneae: Tetragnathidae)

Individuals of the orb-weaving spider Nephila clavipesbuild complex webs with a region used for prey capture, the orb, and tangle webs opposite either face, the barrier webs. Barrier webs have been hypothesized to serve a variety of functions, including predator defense, and the primary function of the barrier web should be reflected in the relative size of the barrier to the orb under varying conditions of foraging success and predation risk. To investigate the effects of predation pressure and foraging success on barrier web structure, I conducted a comparative study in three disjunct populations that differed in predation risk and foraging success. Although both the orb web and the barrier webs are silk, there was no indication of a foraging-defense trade-off. Barrier web structure did not change during seasonal shifts in orb web size related to changes in preycapture rate, and barrier web silk density and orb radius were positively correlated. The hypothesis that the construction of barrier webs is in part a response to predation pressure was supported. Barrier webs do deflect attacks by some predators, and barrier webs built by small spiders, suffering frequent predation attempts, had a higher silk density than barrier webs built by larger individuals. Additionally, barrier web complexity decreased at a later age in areas with higher predation risk.     

Are three‐dimensional spider webs defensive adaptations?

Spider webs result from complex behaviours that have evolved under many selective pressures. Webs have been primarily considered to be foraging adaptations, neglecting the potential role of predation risk in the evolution of web architecture. The ecological success of spiders has been attributed to key innovations in how spiders use silk to capture prey, especially the invention of chemically adhesive aerial two‐dimensional orb webs. However, araneoid sheet web weavers transformed the orb architecture into three‐dimensional webs and are the dominant group of aerial web‐building spiders world‐wide, both in numbers and described species diversity. We argue that mud‐dauber wasps are major predators of orbicularian spiders, and exert a directional selective pressure to construct three‐dimensional webs such that three‐dimensional webs are partly defensive innovations. Furthermore, patterns of diversification suggest that escape from wasp predators may have facilitated diversification of three‐dimensional web‐building spiders.     

Spider capture silk: performance implications of variation in an exceptional biomaterial

Spiders and their silk are an excellent system for connecting the properties of biological materials to organismal ecology. Orb-weaving spiders spin sticky capture threads that are moderately strong but exceptionally extensible, resulting in fibers that can absorb remarkable amounts of energy. These tough fibers are thought to be adapted for arresting flying insects. Using tensile testing, we ask whether patterns can be discerned in the evolution of silk material properties and the ecological uses of spider capture fibers. Here, we present a large comparative data set that allows examination of capture silk properties across orb-weaving spider species. We find that material properties vary greatly across species. Notably, extensibility, strength, and toughness all vary approximately sixfold across species. These material differences, along with variation in fiber size, dictate that the mechanical performance of capture threads, the energy and force required to break fibers, varies by more than an order of magnitude across species. Furthermore, some material and mechanical properties are evolutionarily correlated. For example, species that spin small diameter fibers tend to have tougher silk, suggesting compensation to maintain breaking energy. There is also a negative correlation between strength and extensibility across species, indicating a potential evolutionary trade-off. The different properties of these capture silks should lead to differences in the performance of orb webs during prey capture and help to define feeding niches in spiders.     

Do stabilimenta in orb webs attract prey or defend spiders?

Orb-weaving spiders are ideal organisms for the study of conflictbetween behavioral investments in foraging and defense becausetheir webs provide physical manifestations of those investments.We examined the impact of including stabilimenta, designs ofbright-white noncapture silk, at the center of orb webs forforaging and defense in Argiope aurantia. Our findings suggestthat stabilimentum building is a defensive behavior, supportingthe "web advertisement" hypothesis that the high visibilityof stabilimenta can prevent birds from flying through webs.Yet, spiders often do not include stabilimenta in their webs,indicating that a serious cost is associated with them. We alsoshow, through comparison of paired webs with and without stabilimenta,that stabilimenta reduce the prey capture success of spidersby almost 30%. This demonstrates the potential impact that defensivebehaviors of spiders can have on their foraging success andsuggests that much of the variation in stabilimenta may be accountedfor by a cost—benefit trade-off made when including stabilimentain webs.     

Stabilimenta of Philoponella vicina (Araneae: Uloboridae) and Gasteracantha cancriformis (Araneae: Araneidae): Evidence Against a Prey Attractant Function

Both the uloborid Philoponella vicina and the araneid Gasteracantha cancriformis spiders sometimes placed silk stabilimenta on non-orb "resting webs" that consisted of only one or a few lines. These webs completely lacked sticky silk, so their stabilimenta could not function to attract prey. Some non-orbs were built by spiders when their orb webs are damaged. These observations contradict the prey attraction camouflage hypothesis for stabilimentum function, but are compatible with the spider camouflage and web advertisement to avoid web destruction hypotheses.     

Herbivory in Spiders: The Importance of Pollen for Orb-Weavers

Orb-weaving spiders (Araneidae) are commonly regarded as generalist insect predators but resources provided by plants such as pollen may be an important dietary supplementation. Their webs snare insect prey, but can also trap aerial plankton like pollen and fungal spores. When recycling their orb webs, the spiders may therefore also feed on adhering pollen grains or fungal spores via extraoral digestion. In this study we measured stable isotope ratios in the bodies of two araneid species (Aculepeira ceropegia and Araneus diadematus), their potential prey and pollen to determine the relative contribution of pollen to their diet. We found that about 25% of juvenile orb-weaving spiders’ diet consisted of pollen, the other 75% of flying insects, mainly small dipterans and hymenopterans. The pollen grains in our study were too large to be taken up accidentally by the spiders and had first to be digested extraorally by enzymes in an active act of consumption. Therefore, pollen can be seen as a substantial component of the spiders’ diet. This finding suggests that these spiders need to be classified as omnivores rather than pure carnivores.     

Mesh Width Influences Prey Retention in Spider Orb Webs

Orb‐weaving spiders depend upon the sticky capture spirals of webs to retain insects long enough to be captured. However, insects often escape from orb webs before the spiders can attack them. Therefore, the architectures of orb webs likely reflect strong selective pressure to increase retention times of insects. We experimentally increased the mesh width of one side of an orb web while maintaining the original mesh width on the other side as a control, and then tested the effect of this manipulation on the retention times of four different taxa of insects. We found evidence that increased mesh width of Argiope aurantia orb webs resulted in a general reduction in the retention times of insects. However, retention times for different taxa of insects were not predicted by any one specific morphological or flight characteristic. The influence of mesh width on the retention times of insects is very complex, but our results suggest that mesh width can act to selectively favor the capture of certain taxa of insect prey over others. This effect may help to explain both species level differences in web‐building behaviors and variation in the architectures of webs spun by individual spiders on different days.     

Environmentally induced post‐spin property changes in spider silks: influences of web type,spidroin composition and ecology

Many spiders use silk to construct webs that must function for days at a time, whereas many other species renew their webs daily. The mechanical properties of spider silk can change after spinning under environmental stress, which could influence web function. We hypothesize that spiders spinning longer‐lasting webs produce silks composed of proteins that are more resistant to environmental stresses. The major ampullate (MA) silks of orb web spiders are principally composed of a combination of two proteins (spidroins) called MaSp1 and MaSp2. We expected spider MA silks dominated by MaSp1 to have the greatest resistance to post‐spin property change because they have high concentrations of stable crystalline β‐sheets. Some orb web spiders that spin three‐dimensional orb webs, such as Cyrtophora, have MA silks that are predominantly composed of MaSp1. Hence, we expected that the construction of three‐dimensional orb webs might also coincide with MA silk resistance to post‐spin property change. Alternatively, the degree of post‐spin mechanical property changes in different spider silks may be explained by factors within the spider's ecosystem, such as exposure to solar radiation. We exposed the MA silks of ten spider species from five genera (Nephila, Cyclosa, Leucauge, Cyrtophora, and Argiope) to ecologically high temperatures and low humidity for 4 weeks, and compared the mechanical properties of these silks with unexposed silks. Using species pairs enabled us to assess the influence of web dimensionality and MaSp composition both with and without phylogenetic influences being accounted for. We found neither the MaSp composition nor the three‐dimensionality of the orb web to be associated with the degree of post‐spin mechanical property changes in MA silk. The MA silks in Leucauge spp. are dominated by MaSp2, which we found to have the least resistance to post‐spin property change. The MA silk in Argiope spp. is also dominated by MaSp2, but has high resistance to post‐spin property change. The ancestry of Argiope is unresolved, but it is largely a tropical genus inhabiting hot, open regions that present similar stressors to silk as those of our experiment. Ecological factors thus appear to influence the vulnerability of orb web spider MA silks to post‐spin property change. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 580–588.     

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.     

Testing the Functions of Detritus Stabilimenta in Webs of Cyclosa fililineata and Cyclosa morretes (Araneae: Araneidae): Do They Attract Prey or Reduce the Risk of Predation?

Spiders of the genus Cyclosa often add prey remains and other debris to their orb‐webs. The function of silk decorations is generally associated with defense against predators or with the attraction of prey, but few studies have focused on stabilimenta containing detritus. In this study, we used artificial webs with and without the detritus stabilimenta of two species of Cyclosa to investigate whether these structures increase the number of insects intercepted. Artificial models of spiders and stabilimenta were used to compare the frequency of attacks against different shapes. We also conducted choice experiments in laboratory to determine whether detritus columns attracted Drosophila melanogaster (Diptera: Drosophilidae) and Trigona angustula (Hymenoptera: Apidae, Meliponinae) to the webs. The frequency of interception in artificial webs with a stabilimentum was similar to that of webs without such structure. The taxonomic composition and biomass of insects were also similar in both types of artificial webs. The choice experiments showed no significant tendency in attraction to webs with a stabilimentum. However, models of spiders were attacked at a higher frequency than those simulating detritus columns and silk decorations. These findings argue against the prey attraction hypothesis and suggest that the addition of stabilimenta to webs of Cyclosa could reduce the intensity of predation, possibly by disrupting the image of the spider's outline.     

Fine structure of sheet-webs of Linyphia triangularis (Clerck) and Microlinyphia pusilla (Sundevall), with remarks on the presence of viscid silk

We examined the webs of Linyphia triangularis (Clerck) and Microlinyphia pusilla (Sundevall) using light and scanning electronic microscopic techniques and compared them with the better known orb‐webs. The linyphiid sheet‐web consists of an unordered meshwork of fibres of different thicknesses. The sheet is connected to the scaffolding by means of attachment discs. Thin threads with globules, which appear similar to the viscid silk droplets of orb‐webs, are present in most webs examined. Webs of M. pusilla had a higher density of these globules than did webs of L. triangularis. Webs of both species possess five types of thread connections and contain no aqueous glue for prey capture. Instead, unlike orb‐webs, the sticky substances produced by the linyphiid aggregate glands cement the different layers and threads of the sheet by drying up after being produced. Due to their function, sheet webs may not require viscid silk, thereby leading to a more economic web. The assumption made in most previous studies, that the globules in linyphiid webs have the same properties and function as viscid silk in orb‐webs, is unfounded.     

The biology of Pholcus phalangioides (Araneae, Pholcidae): predatory versatility, araneophagy and aggressive mimicry

Predatory versatility occurs in Pholcus phalangioides (Fuesslin). In addition to building prey-catching space webs, P. phalangioides invades webs of other spiders and feeds on the occupants. It acts as an aggressive mimic by performing specialized vibratory behaviours to which the prey-spider responds as it normally would to its own prey. Prey (spiders and insects) is attacked by wrapping. Prey that trips over lines at the edge of a web of P. phalangioides , but fails to enter the web, is successfully attacked: P. phalangioides leans out of its web to throw silk over the prey, keeping as few as two legs on the silk. However, P. phalangioides does not attack prey that is completely away from webs. Occasionally, P. phalangioides feeds on eggs of other spiders and on ensnared insects it encounters in alien webs. Experimental evidence indicates that vision is of little or no importance in the predatory behaviour of P. phalangioides . Although P. phalangioides invades diverse types of webs, in addition to using its own web, its efficiency as a predator varies with web-type. It is most efficient as a predator of spiders and, especially, insects on its own web, and least efficient as a predator of amaurobiids on their cribellate sheet webs. Sensory, locomotory and other factors which influence differential predatory efficiency are discussed. The behaviour of P. phalangioides is compared to that of Portia , an araneophagic web-invading salticid, and the results of this study are discussed in relation to hypotheses concerning salticid evolution.     

蜘蛛位置对成功捕获猎物和球型网图案的影响

静坐在球型网的中心,蜘蛛可能遭受天敌的攻击并暴露在不利的天气条件下,如风和雨。然而,栖居于网的中心使蜘蛛比隐藏在隐蔽场所中的蜘蛛能更迅速地察觉并捕获猎物,这是因为猎物的位置仅能被位于网中心的蜘蛛所确定。对在隐蔽场所中的蜘蛛而言,提高对猎物捕获率的方式之一是尽量减少隐蔽所与网中心的距离。而且,网中心与隐蔽所之间较短的距离使蜘蛛能更迅速地逃离危险境况。我使用既在网中心、又在隐蔽场所的硬类肥蛛(Larinioides sclopetarius Clerck),来检验这两种行为如何影响对猎物的捕获成功率。隐藏在隐蔽场所中的蜘蛛更经常忽略猎物,使猎物也有比较多的逃离机会,这样,与在网中心的蜘蛛相比,猎物的损失率就更高。另外,研究了隐蔽场所的位置对球型网图案的影响。在大多数球型网中,网中心上方的区域比网下方小,丝也比较少,形成了结构不对称的网;隐蔽场所通常在网的上方。当隐蔽场所的位置在实验中被倒转时,就形成了非典型的球型网。最后,L．sclopetarius建造的网有很突出的边缘非对称性,与隐蔽场所相邻的区域面积较小,而远离隐蔽场所的区域面积较大,这也可解释为减少了隐蔽场所和网中心之间的距离[动物学报50(4)：559-565．2004]。     

2种织圆网蜘蛛个体大小与蛛网粘丝区面积间关系

在不惊扰蜘蛛的情况下对悦目金蛛Argiope amoena和圆尾肖蛸Tetragnatha vermiformis的个体大小与蛛网粘丝区面积问的相关性进行了野外观察。主要测量了蜘蛛体长、蛛网粘丝区直径、蛛网框丝固着点间最大距离、网中枢到地面或水面距离、网平面与水平线的夹角等参数;另外还对蛛网框丝固着点间最大距离作为圆网蛛网址选择行为量化指标的可行性进行了探讨。结果表明,2种蜘蛛体长与蛛网粘丝区面积以及蜘蛛体长与蛛网框丝固着点间最大距离均呈现明显的正相关。悦目金蛛体长与蛛网粘丝区面积的相关性高于圜尾肖蛸,这可能与悦目金蛛在其生境中易于找到框丝固着点、而圆尾肖蛸在其生境中较难找到框丝同着点有关;     

Signal conflict in spider webs driven by predators and prey

Variation in the sensory physiologies of organisms can bias the receptions of signals, driving the direction of signal evolution. Sensory drive in the evolution of signals may be particularly important for organisms that confront trade-offs in signal design between the need for conspicuousness to allow effective transfer of information and the need for crypsis of the signal to unintended receivers. Several genera of orb-weaving spiders include conspicuous silk designs, stabilimenta, in the centre of their webs. Stabilimenta can be highly visible signals to predators, warning them of the presence of a noxious, sticky silk web. However, stabilimenta can also be used by prey as a signal in avoidance of webs, creating a trade-off in signal visibility. I argue that the derived spectral properties of stabilimentum silk have resulted in part from this conflict. The innate colour preferences of insects, their ability to learn colours, and the spectral properties of flowers all suggest that the reflectance spectra of stabilimenta renders them relatively cryptic to many insect prey, while maintaining their visibility to vertebrate predators.