Brent D. Opell

TESTING ADAPTIVE RADIATION AND KEY INNOVATION HYPOTHESES IN SPIDERS

We combine statistical and phylogenetic approaches to test the hypothesis that adaptive radiation and key innovation have contributed to the diversity of the order Araneae. The number of unbalanced araneid clades (those whose species numbers differ by 90% or more) exceeds the number predicted by a null Markovian model. The current phylogeny of spider families contains 74 bifurcating nodes, of which 31 are unbalanced. As this is significantly more than the 14.8 expected unbalanced nodes, some of the diversity within the Araneae can be attributed to some deterministic cause (e.g., adaptive radiation). One of the more highly unbalanced (97%) bifurcations divides the orb‐weaving spiders into the Deinopoidea and the larger Araneoidea. A simple statistical model shows that the inequality in diversity between the Deinopoidea and the Araneoidea is significant, and that it is associated with the replacement of primitive cribellar capture thread by viscous adhesive thread and a change from a horizontal to a vertical orb‐web orientation. These changes improve an orb‐webs ability to intercept and retain prey and expand the adaptive zone that orb‐weaving spiders can occupy and are, therefore, considered to be “key innovations.”

van der Waals and hygroscopic forces of adhesion generated by spider capture threads

SUMMARY Cribellar thread is the most primitive type of sticky prey capture thread found in aerial spider webs. Its outer surface is formed of thousands of fine fibrils that issue from a cribellum spinning field. The fibrils of primitive cribellar thread are cylindrical, whereas those of derived threads have nodes. Cribellar threads snag on insect setae but also adhere to smooth surfaces. A previous study showed empirically that cylindrical fibrils use only van der Waals forces to stick to smooth surfaces, as their stickiness is the same under different humidity. By contrast, noded fibrils are stickier under high humidity, where they are presumed to adsorb atmospheric water and implement hygroscopic (capillary) adhesion. Here, we model thread stickiness according to these two adhesive mechanisms. These models equate stickiness with the force necessary to overcome the adhesion of fibril contact points in a narrow band along each edge of the contact surface and to initiate peeling of the thread from the surface. Modeled and measured thread stickiness values are similar, supporting the operation of the hypothesized adhesive forces and portraying an important transition in the evolution of spider threads. Cribellar threads initially relied only on van der Waals forces to stick to smooth surfaces. The appearance of fibril nodes introduced hydrophilic sites that implemented hygroscopic force and increased thread stickiness under intermediate and high humidity.

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.

The effect of insect surface features on the adhesion of viscous capture threads spun by orb-weaving spiders

SUMMARY Spider orb-webs intercept a broad range of insects and their capture threads must adhere to a range of surface textures. In species of the Araneoidea clade, these capture threads are composed of viscid droplets whose size and spacing differ among species. To determine how droplet profile and insect surface texture interact, we measured the stickiness of viscous threads produced by four species using four insect surfaces that ranged from a smooth beetle elytra to the dorsal surface of a fly abdomen that was covered by large, widely spaced setae. The adhesion of threads to these surfaces differed by as much as 3.5-fold within a spider species and 2.1-fold for the same insect surface between spider species. However, 96% of these differences in stickiness was explained by four variables: the ratio of natural log of droplet volume to setal length, the natural log of droplet volume per mm of thread length, setal surface area, and the area of cuticle not excluded from thread contact by setae. Compared with previous measurements of primitive cribellar capture threads produced by orb weavers of the Deinopoidea clade, viscous threads performed more uniformly over the range of insect surfaces. They also held bug hemelytra, which were densely covered with fine setae, more securely, but held beetle elytra, fly wings and fly abdomens less securely than did viscous threads. Hemelytra may be held more securely because their setae more easily penetrate the viscous boundary layer to establish a greater area of interaction and, after having done so, offer more resistance as they are pulled through this layer. Finely textured surfaces may also have higher effective surface energies and therefore may interact more completely with viscous material.

Functional Similarities of Spider Webs with Diverse Architectures

Spider orb webs are made of sticky prey capture threads supported by a scaffold of nonsticky threads. Capture threads produced by members of the family Uloboridae are formed of thousands of dry, proteinaceous silk fibrils. From measurements of the diameters and lengths of fibers that form the sticky and nonsticky threads of uloborids, this study determines the volume of silk these webs contain. It employs a transformational analysis to examine the relationship between spider size and the silk volume and total stickiness of webs produced by four orb-weaving species and four species that spin simpler webs. Despite differences in web design, web-monitoring behavior, and spider size, a webs total silk volume is directly related to spider weight. A webs prey capture potential, as determined by its total stickiness and total capture area, is also directly related to spider weight. The volume of silk fibrils responsible for a webs stickiness is related to spider weight, whereas the volume of its support elements is not but appears instead to be influenced by web orientation and architecture. Thus, a spiders energetic requirements appear to set the bounds within which the material investment, stickiness, and architectural details of its web are free to differ.

Environmental response and adaptation of glycoprotein glue within the droplets of viscous prey capture threads from araneoid spider orb-webs

SUMMARY Viscous threads that form the prey capture spiral of araneoid orb-webs retain insects that strike the web, giving a spider more time to locate and subdue them. The viscoelastic glycoprotein glue responsible for this adhesion forms the core of regularly spaced aqueous droplets, which are supported by protein axial fibers. Glycoprotein extensibility both facilitates the recruitment of adhesion from multiple droplets and dissipates the energy generated by insects struggling to free themselves from the web. Compounds in the aqueous material make the droplets hygroscopic, causing an increase in both droplet volume and extensibility as humidity (RH) rises. We characterized these humidity-mediated responses at 20%, 37%, 55%, 72% and 90% RH in two large orb-weavers, Argiope aurantia, which is found in exposed habitats, and Neoscona crucifera, which occupies forests and forest edges. The volume-specific extension of A. aurantia glycoprotein reached a maximum value at 55% RH and then declined, whereas that of N. crucifera increased exponentially through the RH range. As RH increased, the relative stress on droplet filaments at maximum extension, as gauged by axial line deflection, decreased in a linear fashion in A. aurantia, but in N. crucifer increased logarithmically, indicating that N. crucifera threads are better equipped to dissipate energy through droplet elongation. The greater hygroscopicity of A. aurantia threads equips them to function in lower RH environments and during the afternoon when RH drops, but their performance is diminished during the high RH of the morning hours. In contrast, the lower hygroscopicity of N. crucifera threads optimizes their performance for intermediate and high RH environments and during the night and morning. These interspecific differences support the hypothesis that viscous capture threads are adapted to the humidity regime of an orb-weavers habitat.

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 spiders 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.

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.

ESTIMATING THE STICKINESS OF INDIVIDUAL ADHESIVE CAPTURE THREADS IN SPIDER ORB WEBS

Abstract Sticky threads improve an orb webs ability to retain the insects that strike it, allowing a spider more time to subdue these insects before they can escape from the web. The adhesive capture threads found in most orb webs feature small droplets of aqueous material. Inside each droplet, glycoprotein granules coalesce to impart thread stickiness. An independent contrast analysis of threads produced by the adults of five species (Leucauge venusta, Argiope trifasciata, Micrathena gracilis, Cyclosa conica, Araneus marmoreus) and ontogenetic studies of the threads of two of these species show that the volume of material in a threads droplets is directly related to its stickiness. Models based on these analyses predict thread stickiness to within an average of 11% of the mean measured values using measurements of droplet diameter and distribution that are easily made with a compound microscope. This approach will facilitate the inclusion of thread stickiness in studies that examine the properties and performance of spider orb-webs.

THE RESPIRATORY COMPLEMENTARITY OF SPIDER BOOK LUNG AND TRACHEAL SYSTEMS

Like most spiders, members of the orb‐weaving family Uloboridae have a dual respiratory system. Book lungs oxygenate the hemolymph and tracheae carry oxygen directly to tissues. Most members of the family are characterized by an extensive tracheal system that extends into the prosoma, where branches enter the legs. A comparison of both absolute and size‐specific indices of these two respiratory components in six uloborid species using the independent contrast method shows that their development is inversely related and indicates that these two systems are complementary. Species that more actively monitor reduced webs have tracheae with greater cross sectional areas and book lungs with smaller areas than do orb‐weaving species that less aggressively manipulate their webs. Thus, the acuteness of a spiders oxygen demands appears to influence the development of its respiratory components. As the tracheae assume more responsibility for providing oxygen the book lungs become less well developed and vice versa. J. Morphol. 236:57–64, 1998.