Glandular quinoline-derivates protect crustacean woodlice from spider predation

Abstract

In evolutionary time, aquatic crustaceans colonized land and faced new terrestrial predators such as spiders and ants. We tested the hypothesis that the crustacean terrestrial woodlouse Porcellio scaber produces defensive metabolites that provide protection against terrestrial predators. When attacked by a predator, P. scaber expels proteinaceous secretions from its tegumental glands. Analyses of gland secretion extracts by gas chromatography-mass spectrometry and by liquid chromatography-mass spectrometry revealed four metabolites: methyl 8-hydroxy-quinoline-2-carboxylate, methyl 8-hydroxy-4-methoxy-quinoline-2-carboxylate, methyl 8-(sulfooxy)quinoline-2-carboxylate and methyl 4-methoxy-8-(sulfooxy)quinoline-2-carboxylate, the latter three being natural products not previously known. In behavioural experiments, Steatoda grossa spiders readily preyed on Tenebrio molitor beetles but avoided chemically well-defended P. scaber. When beetles were rendered chemically well-defended by topical applications of either P. scaber gland secretion extract or synthetic metabolites identified in these extracts, spiders rejected the beetles as prey. Our data support the hypothesis that P. scaber produces defensive metabolites against terrestrial predators. We show that the crustacean P. scaber, like many insects, is chemically defended against predators.

Keywords: Oniscidia; antipredator trait; chemical ecology; spider.

Figure 1.

Chromatographic-mass spectrometric analyses of defensive secretions of Porcellio scaber. (a) Total ion chromatogram (TIC) of GC-MS. (b, c) Electron ionization spectra of (b) methyl 8-hydroxy-quinoline-2-carboxylate (1) and (c) methyl 8-hydroxy-4-methoxy-quinoline-2-carboxylate (2). (d) TIC of HPLC-MS. (e−h) Electrospray ionization spectra of (e, f) methyl 8-(sulfooxy)quinoline-2-carboxylate (9) and 1, and of (g, h) methyl 4-methoxy-8-(sulfooxy)quinoline-2-carboxylate (10) and 2.

Figure 2.

Effects of (i) prey type (chemically well-defended P. scaber woodlice or chemically less defended T. molitor beetles) and (ii) prey treatment (topical application of beetles with P. scaber gland secretion, synthetic gland metabolites (40 ng) or a water control) on predation by S. grossa false widow spiders. Bars indicate the number of prey being preyed upon and killed (right of 0), or not (left of 0), by the spiders. Metabolites: 1 = methyl 8-hydroxy-quinoline-2-carboxylate; 2 = methyl 8-hydroxy-4-methoxy-quinoline-2-carboxylate; 9 = methyl 8-(sulfooxy)quinoline-2-carboxylate; 10 = methyl 4-methoxy-8-(sulfooxy)quinoline-2-carboxylate. An asterisk (*) denotes a statistically significant difference (Fisher’s exact tests; p < 0.05).