Humidity-mediated changes in an orb spider's glycoprotein adhesive impact prey retention time

Abstract

Properties of the viscous prey capture threads of araneoid orb spiders change in response to their environment. Relative humidity (RH) affects the performance of the thread's hygroscopic droplets by altering the viscoelasticity of each droplet's adhesive glycoprotein core. Studies that have characterized this performance used smooth glass and steel surfaces and uniform forces. In this study, we tested the hypothesis that these changes in performance translate into differences in prey retention times. We first characterized the glycoprotein contact surface areas and maximum extension lengths of Araneus marmoreus droplets at 20%, 37%, 55%, 72% and 90% RH and then modeled the relative work required to initiate pull-off of a 4 mm thread span, concluding that this species' droplets and threads performed optimally at 72% RH. Next, we evaluated the ability of three equally spaced capture thread strands to retain a house fly at 37%, 55% and 72% RH. Each fly's struggle was captured in a video and bouts of active escape behavior were summed. House flies were retained 11 s longer at 72% RH than at 37% and 55% RH. This difference is ecologically significant because the short time after an insect strikes a web and before a spider begins wrapping it is an insect's only opportunity to escape from the web. Moreover, these results validate the mechanism by which natural selection can tune the performance of an orb spider's capture threads to the humidity of its habitat.

Linking properties of an orb‐weaving spider's capture thread glycoprotein adhesive and flagelliform fiber components to prey retention time

“…A pooled sample of 30 adult flies had a mean mass of 12.03 mg per fly, very similar to the 12.01 mg mean fly mass of our previous study (Opell et al, ). A sample 10 flies from the current study were also similar in size to a sample of six flies from the previous study (values in parentheses): head width across eyes = 2,185 µm ± 40 µm standard error (2,220 µm ± 40 µm) and notum width = 2,116 µm ± 40 µm (2,110 µm ± 70 µm), neither measurement differing significantly ( t test p = .4966 and .9650, respectively).…”

“…These include web orientation (horizontal vs. vertical), velocity of insect impact, the number of capture spirals contacted, the surface texture of the insect body regions that contact capture threads, the insect's struggle behavior, and whether or not an insect readheres to capture threads after pulling free of one set of threads and tumbling into lower capture thread spirals of a vertical orb web (Blackledge & Zevenbergen, ; Opell & Schwend, ; Zschokke & Nakata, ). As in the previous study of A. marmoreus (Opell et al, ), we attempted to control for as many of these variables as possible by preparing three horizontally oriented capture thread arrays from each spider's web sample and by placing an anesthetized adult Musca domestica Linnaeus, 1758 housefly wings downward on the center of each array.…”

“…We monitored temperature using a thermometer suspended 1 cm below the top of each chamber and maintained at 23°C to standardize our observations to both the previous insect retention study (Opell et al, ) and studies of capture thread droplet properties (Opell, Clouse, & Andrews, ; Opell et al, ; Stellwagen, Opell, & Clouse, , ; Stellwagen et al, ). To 37% RH and 72% RH chambers, we added a 22 × 15 cm aluminum heat sink that extended 11 cm into the top of the chamber and served to dissipate the heat added by the dehumidifier and humidifier, respectively.…”

“…Thus, a fly's behavior was summarized as total number of activity bouts, total leg struggle time, total wing flap time, and total active struggle time. To account for interindividual variance in capture thread adhesion, we also followed the approach used in our previous study (Opell et al, ), computing the mean leg struggle, wing flap time, and total active struggle time for the three humidities for each individual and then, for each humidity, determining the deviation of each index from its respective mean value. Thus, a retention time less than meantime would have a negative value and one greater than the mean a positive value.…”

“…The previously studied species, Araneus marmoreus , builds webs in forest edge vegetation, where humidity does not drop greatly during late morning and afternoon (Opell, Buccella, Godwin, Rivas, & Hendricks, ). In the current study, we examined the effect of humidity on housefly retention by threads of the sympatric species A. aurantia and A. trifasciata , large orb weavers that construct webs in exposed, grassy and weedy habitats and are widely distributed in United States (Levi, ).…”