Life as a fortress – structure, function, and adaptive values of morphological and chemical defense in the oribatid mite Euphthiracarus reticulatus (Actinotrichida)

Background: Oribatid mites are among the primordial decomposer faunal elements and potential prey organisms insoil. Among their myriad morphological defenses are strong sclerotization and mineralization, cuticular tecta, and the “ptychoid” body-form, which allows to attain an encapsulated, seed-like appearance. Most oribatid mites possess a pair of exocrine glands that produce blends of hydrocarbons, terpenes, aromatics, alkaloids and cyanogenic compounds.Many species evolved “holistic” defensive strategies by combining several morphological and chemical traits. Methods: We describe the morphological and chemical bases of defense in the ptychoid oribatid Euphthiracarus reticulatus. The functional morphology was investigated with synchrotron X-ray microtomography (SRμCT) and highspeed life-radiography. Gland secretions were collected from 20,000 adult specimens, purified and fractionated by preparative capillary gas chromatography (pcGC) and analyzed by gas chromatography / mass spectrometry (GC/MS), high-resolution mass spectrometry (HRMS), and nuclear magnetic resonance spectroscopy (NMR). The adaptive values of morphological and chemical defenses were estimated in bioassays against three predators: a similar-sized gamasid mite (Stratiolaelaps miles, ca. 0.8 mm, with slender chelicera for piercing membranous cuticular regions), and two larger staphylinid beetles, Stenus juno (ca. 7 mm, bearing a harpoon-like sticky labium and sickle-shaped mandibles) and Othius punctulatus (ca. 14 mm, bearing plesiomorphic chewing mandibles). Results: The secretions comprised two components: the diterpene β-springene and a novel compound with a mass of 276 g/mol – eventually elucidated as 2-(but-1-en-1-yl)-4-butylidene-3-(pent-2-en-1-yl)-pentanedial, to which we assign the trivial name δ-acaridial. Upon attacks by S. juno, E. reticulatus reacted quickly: within 150 ms from the first contact the encapsulation was almost completed – less time than the beetle needed to retract the labium and transfer the mite to the mandibles. Chemically-defended specimens of E. reticulatus effectively repelled all predators. After depletion of oil-gland reservoirs, however, O. punctulatus easily fed on the mites while S. miles and S. juno were not able to overcome the morphological barrier of strong cuticle and ptychoid body form. Conclusion: Such an effective, holistic defense strategy, involving both morphological and chemical traits, probably carries high resource-costs, but it allows adult euphthiracaroid mites to occupy an almost “enemy-free space” despite the high diversity of predators in soil.