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

Date Published: February 3, 2017

Publisher: Public Library of Science

Author(s): Thiago Gechel Kloss, Marcelo Oliveira Gonzaga, Leandro Licursi de Oliveira, Carlos Frankl Sperber, Peter Schausberger.

http://doi.org/10.1371/journal.pone.0171336

Abstract

Some ichneumonid wasps induce modifications in the web building behavior of their spider hosts to produce resistant “cocoon” webs. These structures hold and protect the wasp’s cocoon during pupa development. The mechanism responsible for host manipulation probably involves the inoculation of psychotropic chemicals by the parasitoid larva during a specific developmental period. Recent studies indicate that some spiders build cocoon webs similar to those normally built immediately before ecdysis, suggesting that this substance might be a molting hormone or a precursor chemical of this hormone. Here, we report that Cyclosa spider species exhibiting modified behavior presented higher 20-OH-ecdysone levels than parasitized spiders acting normally or unparasitized individuals. We suggest that the lack of control that spiders have when constructing modified webs can be triggered by anachronic activation of ecdysis.

Partial Text

Parasites and parasitoids often alter specific behaviors of their hosts. Examples of changes range from subtle shifts in one aspect of the host’s behavior to the performance of completely novel and complex behavioral patterns [1]. Some of these changes might be primarily due to the host’s own defensive responses to infection [1,2] or to exploitation of the host’s nutritional resources by the parasites [3]. Others changes in behavior are classified as host manipulation to acquire some benefit in survivorship or dispersal ability [1]. In the majority of manipulation cases, however, little is known about the proximal mechanisms responsible for behavioral alterations [4]. For example, the cricket Nemobius sylvestris (Bosc, 1792) performs the unusual behavior of searching for water and jumping into it after being attacked by mature individuals of the hairworm Paragordius tricuspidatus (Dufour, 1828). This behavior is induced by the parasite producing protein from the Wnt family, which act on the central nervous system of the host [5]. Another reported case of host manipulation involves the injection of venom containing a dopamine-like substance into the cerebral ganglia of the cockroach Periplaneta americana (Linnaeus, 1758) by the parasitoid wasp Ampulex compressa (Fabricius, 1781). This action directly stimulates the grooming-releasing circuits within the host’s cerebral ganglia, which enters into a subsequent nonparalytical hypokinetic state [6,7].

For both spiders species, C. morretes and C. fililineata, the molting web showed a simplification in its structure, characterized by absence of spirals and reduction in the number of radii to less than ten (C. morretes: 8.8 ± 0.5, n = 10 and C. fililineata: 8.0 ± 0.5, n = 5; Fig 1D and 1H). The molting web maintained its modified structure for up to six days (range: 2–6 days; n = 9), while the web-constructing spider remained motionless at the center of the web. During the second day after building the molting web, spiders replaced their exoskeletons.

We verified that the proximal mechanism that triggers the behavioral changes in web building in spiders carrying parasitoid larvae in the third stage of development involve increased 20E levels in the spider host’s hemolymph. Our results reveal that the proximal mechanism that triggers this behavioral change in the host spiders activates similar web building behavior, as occurs in unparasitized, juvenile spiders just before ecdysis. The evidence for this conclusion was the observed similarities between molting and cocoon webs.

 

Source:

http://doi.org/10.1371/journal.pone.0171336

 

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