Glandular quinoline-derivates protect crustacean woodlice from spider predation

In evolutionary time, aquatic crustaceans colonized land and faced new terrestrial predators such as spiders and ants. Working with the crustacean woodlouse Porcellio scaber, we tested the hypothesis that the shift from aquatic to terrestrial habitat prompted the evolution of defensive metabolites against terrestrial predators. When attacked by a predator, P. scaber woodlice expel proteinaceous secretions from their tegumental glands. Analyses of gland secretion extracts by gas chromatography-mass spectrometry and by liquid-chromatography-tandem 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 preyed on chemically undefended Tenebrio molitor beetles but avoided chemically defended P. scaber. When beetles were rendered chemically 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 the evolutionary transition of crustaceans from aquatic to terrestrial habitats prompted the evolution of defensive metabolites against terrestrial predators. We show that crustaceans, like many insects, are chemically defended against predators. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=47 SRC="FIGDIR/small/645209v1_ufig1.gif" ALT="Figure 1"> View larger version (20K): org.highwire.dtl.DTLVardef@1efd0forg.highwire.dtl.DTLVardef@7804acorg.highwire.dtl.DTLVardef@17ad216org.highwire.dtl.DTLVardef@76d666_HPS_FORMAT_FIGEXP M_FIG C_FIG Graphical abstractUnder attack by the predatory spider Steatoda grossa, the crustacean Porcellio scaber releases four defensive 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 previously unknown natural products.