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

Abstract

Background: Oribatid mites are among the primordial decomposer faunal elements and potential prey organisms in soil. 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/moleventually 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 completedless 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.

Under pressure: force resistance measurements in box mites (Actinotrichida, Oribatida)

“…In such scenarios with pronounced predation pressure, oribatid mites developed diverse and effective defensive strategies ([35, 37] and references within), and consequently they are assumed to live in a largely ‘enemy-free space’ [41]. The glandulate Oribatida use chemical defenses that work through the release of secretions by the opisthonotal glands (or ‘oil glands’; [9, 18, 21, 23]) like for example neryl formate, neral, geranial, 2-hydroxy-6-methyl-benzaldehyde (2,6-HMBD; [44]), δ-acaridial [24], and even hydrogen cyanide [10]. Morphological defenses of oribatid mites include a thick, hardened, and in some cases biomineralized cuticle [3, 38, 39], wing-like tecta protecting the legs (pteromorphs; [45, 55]), and erectile setae [36].…”

“…Ptychoidy probably evolved three times independently, in the groups Mesoplophoridae, Protoplophoridae (both belonging to the Enarthronota), and in the well-studied Ptyctima (Mixonomata, Fig. 1a; [24, 47, 50–54, 67]). The latter taxon comprises the two groups Euphthiracaroidea and Phthiracaroidea (Figs.…”

“…Both groups are well protected through ptychoidy from attacks of similar sized predators like Pergamasus septentrionalis O udemans [41], Stratiolaelaps miles B erlese [24], and small predatory beetles [24]. Euphthiracaroidea, however, additionally feature predator-repelling chemical secretions, that are effective against predators larger than the animals themselves [24]. Since Ptyctima evolved within the glandulate group of Oribatida, it seems likely that Phthiracaroidea secondarily reduced the chemical defense [24].…”

“…Euphthiracaroidea, however, additionally feature predator-repelling chemical secretions, that are effective against predators larger than the animals themselves [24]. Since Ptyctima evolved within the glandulate group of Oribatida, it seems likely that Phthiracaroidea secondarily reduced the chemical defense [24]. This hypothesis implies that Phthiracaroidea lost their chemical defense and rely on a hardened notogaster and ptychoidy as defensive systems; so, their effective protection is maintained by an improved mechanical resistance.

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“…Othius punctulatus G oeze (14 mm long) on the other hand can crack chemically undefended (cf. reducible defense in [20]) euphthiracaroid mites, but not phthiracaroid mites similar in size to Euphthiracaroidea [24]. Ptychoidy thus seems to be less effective against large predators in Euphthiracaroidea than in Phthiracaroidea and we assume that their difference in body form is key for understanding the different armament of defensive systems in the two ptyctimous groups.…”