Sean J. Blamires

Plasticity in extended phenotypes: orb web architectural responses to variations in prey parameters

SUMMARY A spider orb web is an extended phenotype; it modifies and interacts with the environment, influencing spider physiology. Orb webs are plastic, responding to variations in prey parameters. Studies attempting to understand how nutrients influence spider orb-web plasticity have been hampered by the inability to decouple prey nutrients from other, highly correlated, prey factors and the intrinsic link between prey protein and prey energy concentration. I analyzed the nutrient concentrations of cockroaches, and adult and juvenile crickets to devise experiments that controlled prey protein concentration while varying prey size, ingested mass, energy concentration and feeding frequency of the orb web spider Argiope keyserlingi. I found that A. keyserlingi alters overall architecture according to feeding frequency. Decoration length was inversely related to ingested prey mass and/or energy density in one experiment but directly related to ingested prey mass in another. These contradictory results suggest that factors not examined in this study have a confounding influence on decoration plasticity. As decorations attract prey as well as predators decreasing decoration investment may, in some instances, be attributable to benefits no longer outweighing the risks. Web area was altered according to feeding frequency, and mesh size altered according to feeding frequency and prey length. The number of radii in orb webs was unaffected by prey parameters. A finite amount of silk can be invested in the orb web, so spiders trade-off smaller mesh size with larger web capture area, explaining why feeding frequency influenced both web area and mesh size. Mesh size is additionally responsive to prey size via sensory cues, with spiders constructing webs suitable for catching the most common or most profitable prey.

Multiple prey cues induce foraging flexibility in a trap-building predator

Predators must be behaviourally flexible to counter the temporal and spatial stochastic fluctuations and response variability of their prey. To ensure behaviours are adequate across environments, animals must regularly assess environmental cues. Spider orb webs are an example of a flexible foraging trait in a predator, as web architectural components vary in response to exposure to different prey types and prey traits. The cues used by orb web spiders to initiate changes in web architecture are not known. Current research predicts that prey nutrients and vibratory stimuli are potential candidates, but how they combine to affect spider foraging decisions is not clear. We performed experiments exposing the giant wood spider, Nephila pilipes, to different prey nutrients and vibratory stimuli. Spiders were fed either large profitable prey with high kinetic energy (crickets) or small prey with low kinetic energy (flies). In two treatments the prey nutrients and vibratory cues came from live prey, but in the other two treatments spiders received dead crickets with webs stimulated by flies and vice versa. The spiders fed on live flies built larger webs with more radii that were less stiff and had greater vibration damping. These web characteristics did not differ between the other three treatment groups. Our results show that in the absence of nutrient and vibratory cues from profitable prey, spiders alter their web architecture to build webs better able to capture the less profitable prey at a cost of more material investment, greater web visibility and reduced vibratory signal clarity.

Prey type, vibrations and handling interactively influence spider silk expression.

SUMMARY The chemical and mechanical properties of spider major ampullate (MA) silks vary in response to different prey, mostly via differential expression of two genes – MaSp1 and MaSp2 – although the spinning process exerts additional influence over the mechanical properties of silk. The prey cues that initiate differential gene expression are unknown. Prey nutrients, vibratory stimuli and handling have been suggested to be influential. We performed experiments to decouple the vibratory stimuli and handling associated with high and low kinetic energy prey (crickets vs flies) from their prey nutrients to test the relative influence of each as inducers of silk protein expression in the orb web spider Nephila pilipes. We found that the MA silks from spiders feeding on live crickets had greater percentages of glutamine, serine, alanine and glycine than those from spiders feeding on live flies. Proline composition of the silks was unaffected by feeding treatment. Increases in alanine and glycine in the MA silks of the live-cricket-feeding spiders indicate a probable increase in MaSp1 gene expression. The amino acid compositions of N. pilipes feeding on crickets with fly stimuli and N. pilipes feeding on flies with cricket stimuli did not differ from each other or from pre-treatment responses, so these feeding treatments did not induce differential MaSp expression. Our results indicate that cricket vibratory stimuli and handling interact with nutrients to induce N. pilipes to adjust their gene expression to produce webs with mechanical properties appropriate for the retention of this prey. This shows that spiders can genetically alter their silk chemical compositions and, presumably, mechanical properties upon exposure to different prey types. The lack of any change in proline composition with feeding treatment in N. pilipes suggests that the MaSp model determined for Nephila clavipes is not universally applicable to all Nephila.

Wind induces variations in spider web geometry and sticky spiral droplet volume

SUMMARY Trap building by animals is rare because it comes at a substantial cost. Using materials with properties that vary across environments maintains trap functionality. The sticky spiral silks of spider orb webs are used to catch flying prey. Web geometry, accompanied by compensatory changes in silk properties, may change across environments to sustain web functionality. We exposed the spider Cyclosa mulmeinensis to wind to test whether wind-induced changes in web geometry are accompanied by changes in aggregate silk droplet morphology, axial thread width or spiral stickiness. We compared: (i) web catching area, (ii) length of total silks, (iii) mesh height, (iv) number of radii, (v) aggregate droplet morphology and (vi) spiral thread stickiness, between webs made by spiders exposed to wind and those made by spiders not exposed to wind. We interpreted co-variation in droplet morphology or spiral stickiness with web capture area, mesh height or spiral length as the silk properties functionally compensating for changes in web geometry to reduce wind drag. Wind-exposed C. mulmeinensis built webs with smaller capture areas, shorter capture spiral lengths and more widely spaced capture spirals, resulting in the expenditure of less silk. Individuals that were exposed to wind also deposited larger droplets of sticky silk but the stickiness of the spiral threads remained unchanged. The larger droplets may be a product of a greater investment in water, or low molecular weight compounds facilitating atmospheric water uptake. Either way, droplet dehydration in wind is likely to be minimized.

Post-secretion processing influences spider silk performance

Phenotypic variation facilitates adaptations to novel environments. Silk is an example of a highly variable biomaterial. The two-spidroin (MaSp) model suggests that spider major ampullate (MA) silk is composed of two proteins—MaSp1 predominately contains alanine and glycine and forms strength enhancing β-sheet crystals, while MaSp2 contains proline and forms elastic spirals. Nonetheless, mechanical properties can vary in spider silks without congruent amino acid compositional changes. We predicted that post-secretion processing causes variation in the mechanical performance of wild MA silk independent of protein composition or spinning speed across 10 species of spider. We used supercontraction to remove post-secretion effects and compared the mechanics of silk in this ‘ground state’ with wild native silks. Native silk mechanics varied less among species compared with ‘ground state’ silks. Variability in the mechanics of ‘ground state’ silks was associated with proline composition. However, variability in native silks did not. We attribute interspecific similarities in the mechanical properties of native silks, regardless of amino acid compositions, to glandular processes altering molecular alignment of the proteins prior to extrusion. Such post-secretion processing may enable MA silk to maintain functionality across environments, facilitating its function as a component of an insect-catching web.

Prey protein influences growth and decoration building in the orb web spider Argiope keyserlingi

Abstract. 1. Protein is important for a foraging animal to consume, as it promotes growth and enhances survival, particularly in web‐building spiders, which need to invest considerable protein into web building and may trade‐off growth for web investment.

Physicochemical Property Variation in Spider Silk: Ecology, Evolution, and Synthetic Production

The unique combination of great stiffness, strength, and extensibility makes spider major ampullate (MA) silk desirable for various biomimetic and synthetic applications. Intensive research on the genetics, biochemistry, and biomechanics of this material has facilitated a thorough understanding of its properties at various levels. Nevertheless, methods such as cloning, recombination, and electrospinning have not successfully produced materials with properties as impressive as those of spider silk. It is nevertheless becoming clear that silk properties are a consequence of whole-organism interactions with the environment in addition to genetic expression, gland biochemistry, and spinning processes. Here we assimilate the research done and assess the techniques used to determine distinct forms of spider silk chemical and physical property variability. We suggest that more research should focus on testing hypotheses that explain spider silk property variations in ecological and evolutionary contexts.

Mechanical Performance of Spider Silk Is Robust to Nutrient-Mediated Changes in Protein Composition

Spider major ampullate (MA) silk is sought after as a biomimetic because of its high strength and extensibility. While the secondary structures of MA silk proteins (spidroins) influences silk mechanics, structural variations induced by spinning processes have additional effects. Silk properties may be induced by spiders feeding on diets that vary in certain nutrients, thus providing researchers an opportunity to assess the interplay between spidroin chemistry and spinning processes on the performance of MA silk. Here, we determined the relative influence of spidroin expression and spinning processes on MA silk mechanics when Nephila pilipes were fed solutions with or without protein. We found that spidroin expression differed across treatments but that its influence on mechanics was minimal. Mechanical tests of supercontracted fibers and X-ray diffraction analyses revealed that increased alignment in the amorphous region and to a lesser extent in the crystalline region led to increased fiber strength and extensibility in spiders on protein rich diets.

A predator's body coloration enhances its foraging profitability by day and night

Few predators forage by both day and night. It remains unknown, however, how the costs and benefits of foraging or signaling are partitioned in animals that forage at all times. The orb-web spider Cyrtophora moluccensis is brightly colored and forages by day and night. We determined the benefits reaped when it forages by both day and night by estimating the biomass of prey caught in their webs. Additionally, we quantified whether the spider’s presence influences the number of prey caught by day and night and whether its colorful body is visible to diurnal and/or nocturnal insects using diurnal and nocturnal insect vision models. We found that approximately five times the biomass of prey was caught in C. moluccensis’ webs by night than by day. Hemipterans, hymenopterans, and dipterans were predominantly caught by day, while lepidopterans (moths) were predominately caught by night. Accordingly, we concluded that foraging by night is more profitable than foraging by day. We predicted that other benefits, for example, energetic advantages or enhanced fecundity, may promote its daytime activity. Foraging success was greater by day and night when the spider was present in the web than when the spider was absent. We also found that parts of the spider’s body were conspicuous to diurnal and nocturnal insects, possibly through different visual channels. The colorful body of C. moluccensis, accordingly, appears to influence its foraging success by attracting prey during both the day and night.

Nutrient-Mediated Architectural Plasticity of a Predatory Trap

Background Nutrients such as protein may be actively sought by foraging animals. Many predators exhibit foraging plasticity, but how their foraging strategies are affected when faced with nutrient deprivation is largely unknown. In spiders, the assimilation of protein into silk may be in conflict with somatic processes so we predicted web building to be affected under protein depletion. Methodology/Principal Findings To assess the influence of protein intake on foraging plasticity we fed the orb-web spiders Argiope aemula and Cyclosa mulmeinensis high, low or no protein solutions over 10 days and allowed them to build webs. We compared post-feeding web architectural components and major ampullate (MA) silk amino acid compositions. We found that the number of radii in webs increased in both species when fed high protein solutions. Mesh size increased in A. aemula when fed a high protein solution. MA silk proline and alanine compositions varied in each species with contrasting variations in alanine between the two species. Glycine compositions only varied in C. mulmeinensis silk. No spiders significantly lost or gained mass on any feeding treatment, so they did not sacrifice somatic maintenance for amino acid investment in silk. Conclusions/Significance Our results show that the amount of protein taken in significantly affects the foraging decisions of trap-building predators, such as orb web spiders. Nevertheless, the subtle differences found between species in the association between protein intake, the amino acids invested in silk and web architectural plasticity show that the influence of protein deprivation on specific foraging strategies differs among different spiders.