Host manipulation by an ichneumonid spider ectoparasitoid that takes advantage of preprogrammed web-building behaviour for its cocoon protection

Abstract

Host manipulation by parasites and parasitoids is a fascinating phenomenon within evolutionary ecology, representing an example of extended phenotypes. To elucidate the mechanism of host manipulation, revealing the origin and function of the invoked actions is essential. Our study focused on the ichneumonid spider ectoparasitoid Reclinervellus nielseni, which turns its host spider (Cyclosa argenteoalba) into a drugged navvy, to modify the web structure into a more persistent cocoon web so that the wasp can pupate safely on this web after the spider's death. We focused on whether the cocoon web originated from the resting web that an unparasitized spider builds before moulting, by comparing web structures, building behaviour and silk spectral/tensile properties. We found that both resting and cocoon webs have reduced numbers of radii decorated by numerous fibrous threads and specific decorating behaviour was identical, suggesting that the cocoon web in this system has roots in the innate resting web and ecdysteroid-related components may be responsible for the manipulation. We also show that these decorations reflect UV light, possibly to prevent damage by flying web-destroyers such as birds or large insects. Furthermore, the tensile test revealed that the spider is induced to repeat certain behavioural steps in addition to resting web construction so that many more threads are laid down for web reinforcement.

Female genital mutilation and monandry in an orb-web spider

“…Some of them were collected as penultimate subadult females, and were kept until they made their final moult. Other adults were collected on their moulting webs, which were characterized by their small size, reduced number of radii, lack of spiral threads and presence of fibrous decorations [13], indicating that the spiders had just moulted to adults. They were convincingly assumed to be virgins, because preliminary observations had revealed that no female mates with a male when on a moulting web.…”

Proximate mechanism of behavioral manipulation of an orb-weaver spider host by a parasitoid wasp

“…The same pattern was observed in C . argenteoalba [18] manipulated by Reclinervellus nielseni (Roman, 1923). In this study, a detailed comparison of web structures, building behavior, and silk spectral/tensile also showed that the few radii of both web types were decorated by many fibrous ultra violet-reflective threads.…”

“…The wasps lay one egg on the spider's abdomen, where the ectoparasitic larva develops by sucking the host’s hemolymph through perforated holes in the spider’s cuticle. Usually, the host spider builds a modified web just before the wasp larva enters the final stage of development [9–18], but, in some cases, the number of radii and spirals of the orb web gradually decrease over several days before the spider dies [19,20]. After the spider builds this modified structure, the larva kills its host, and builds its cocoon attached to the silk threads spun by the host.…”

“…After the spider builds this modified structure, the larva kills its host, and builds its cocoon attached to the silk threads spun by the host. Cocoon webs appear to be more resistant to rupture [18,20,21] and have fewer components (e.g., radii and sticky spirals in orb webs) that are utilized for prey interception and retention. Variations of this general pattern include the addition of barrier threads [22], shorter radii, doubled number of lines in each radius, construction of a reinforced frame [19], reinforcement of the retreat by addition of more threads [14] or a veil sheltering the cavity containing spider and larva [23].…”

“…Modified webs of Cyclosa argenteoalba Bösenberg & Strand, 1906 [18], Allocyclosa bifurca (McCook, 1887) [19], and Nephila clavipes (Linnaeus, 1767) [20] resemble the molting webs spun by unparasitized individuals just before molting. During the molting period, spiders have increasing levels of the hormone 20-OH-ecdysone (20E), which is responsible for renewing their old exoskeletons [24].…”