Feeding mediated web-building plasticity in a cobweb spider

Behavioral plasticity has been proposed as a means by which animals alter their phenotypes in response to changing conditions. Animals may display behavioral plasticity as a consequence of environmental variation. The detritus-based, bell-shaped cobweb spider Campanicola campanulata is an ideal model to study behavioral plasticity, because its web architecture is easy to be quantified, and the functions of different parts of the web are clear. Though the plasticity of cobweb architecture has been reported in a few species, retreats as important defensive structures have rarely been considered before because retreats in most cobwebs are relatively small compared with the web size. We studied the web-building behaviors of C. campanulata under different feeding regimes. We set up 3 spider treatments with different feeding conditions: marginally well fed, moderately well fed, and extremely well fed, and observed the differences in the web architecture among them. In addition, we measured the mechanical properties of anchor silk, and also calculated the foraging and defense investment of the spiders. The results showed that marginally well-fed spiders build cobwebs with significantly longer length of anchor silk, lower retreat to the ground, more number and longer gumfooted lines, and larger capture area, while extremely well-fed spiders build cobwebs with significantly bigger retreat volume and higher height of retreat to the ground. In addition, marginally well-fed spiders invest significantly less during cobweb construction. However, there was no significant difference between the breaking force and elongation at break in anchor silk among different treatments. These results demonstrated that marginally well-fed spiders invest more in foraging, and extremely well-fed spiders invest more in defense, and the spider made a balance between foraging and predator avoidance in response to changes in physiological state. Our study strengthens the current understanding of web construction in cobweb spiders, especially those facing high costs during retreat construction.

Methods
Study species

Campanicola campanulata (Araneae: Theridiidae) is widely distributed in South China, such as Hubei, Zhejiang, and Guizhou provinces (Chen 1993). It builds a web in cool but rain-proofed places such as concaves of rocks or earth walls, or under low overhanging branches (Figure 1A). It feeds mainly on ants, and usually lives in aggregation, building webs solitarily, with 1 spider per retreat (Figure 1B, C). The web consists of anchor silk, a bell-shaped retreat, and dozens of sticky gumfooted lines (Figure 1D). Anchor silks are usually made of strands of silk suspended from concave walls or tree roots. These structures prevent damage to the web by winds. The retreat is made of silk, sand, pebbles, debris, leaves, or shells, and has a small opening at the bottom. Its weight is usually 30–40 times the body weight of the spider. The gumfooted lines of the web emanate from the retreat edge and are fastened to coarse sand grains or fixed substrata, which are mainly used to form a capture web. When ants are intercepted by sticky gumfooted lines, the lines detach from the substrate and pull the prey up toward the retreat, making it difficult for the ants to gain the leverage needed for escape (Argintean et al. 2006). The configuration of the suspended retreat can significantly reduce the spider’s vulnerability to enemies because there are silken tunnels inside the retreat (Henschel and Jocqué 1994), which the enemies cannot tres-pass into. In addition, the sticky gumfooted lines also more or less prevent the invasion of enemies, such as parasitic wasps.

Spider and maintenance

From May to June 2019, we collected sub-adult (i.e., 1 molt before adulthood, ~2.4 mm in body length) C. campanulata from Hubei Dabie Mountain National Nature Reserve in Huanggang, Hubei Province, China (31°5ʹN, 115°48ʹE), and raised them to adulthood in the laboratory. The spiders were maintained individually in a plastic box (length × width × height: 10 cm × 5 cm × 10 cm) with bamboo sticks attached to their inner sides to allow them to build webs. The front and back sides of the box were made of removable transparent Perspex glass. All spiders were kept in the laboratory with controlled environmental conditions (temperature: 25 ± 1 °C; relative humidity: 80  ±  5%; photoperiod: 14 h: 10  h L:D). The bottom of the box was covered with a layer of sand for the spider to collect to build a retreat, and a piece of sponge with absorbed water was placed at the bottom of the box to provide water for the spider. We fed each spider with 2 ants (Monomorium sp., ~2.2mm in body length) every 2 days, and the developmental status (molting) of each spider was checked twice daily (09:00 and 21:00).

Experimental design and procedure

Sixty newly matured female spiders (~2 days after maturity) were randomly divided into 3 treatments (N = 20 in each group): marginally well fed, control (normal feeding, i.e., moderately well fed), and extremely well fed. The body size (carapace width, body length, and body weight) of each spider was measured before the experiment. We fed Monomorium ants to them for 6 days (each spider was fed every 2 days with 2 ants at each time). Then, we measured the morphological parameters of their webs and examined the mechanical properties of the anchor silks (i.e., threads underlying the axial fibers). These data were considered as pretreatment data. After collecting these data, we destroyed all the webs, and let the spiders build new webs in another 6 days, and during this period of time, the spiders were fed differently. According to our field dissection of the retreat of the spiders, we found that the most normally developed adult spiders generally consumed about 6 ants in a week. Therefore, in this study, for those spiders in control treatment (moderately well fed), they were fed every 2 days with 2 ants at each time (6 ants in total). For those spiders in marginally well-fed treatment, they were fed only once with 2 ants (2 ants in total). For those spiders in extremely well-fed treatment, they were fed every 2 days with 5 ants at each time (15 ants in total). We observed and recorded the consuming process to make sure the ants were consumed. After these 6 days of different feedings, we measured the morphological parameters of the webs and examined the mechanical properties of the anchor silks again in each group. These data were considered as posttreatment data.