Welcome to the new version of CaltechAUTHORS. Login is currently restricted to library staff. If you notice any issues, please email coda@library.caltech.edu
Published August 13, 2018 | Supplemental Material + Published
Journal Article Open

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 high-speed 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.

Additional Information

© The Author(s) 2018. Open Access - This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Received: 23 February 2018. Accepted: 15 June 2018. Published online 13 August 2018. Part of the following topical collections: Biotic interactions We thank Thomas van de Kamp, Tomy dos Santos Rolo, and Tomáš Faragó for their help during data acquisition and reconstruction of tomographic data; Norbert Müller and Maria Theresia Pöschko for help in setting up NMR measurements; Herbert Kogler for verifying the structure determination by going through the NMR spectra at the Austrian NMR Summer School; Hans-Jörg Leis and Irmgard Schäffler for their help with HRMS and pcGC, respectively; Wojciech Niedbała for his help in the determination of the species; and Alexander Schneider for his assistance with the Othius punctulatus video recordings. Adrian Brückner was supported by a scholarship for undergraduate students, a PhD grant, and two short-term research stipends provided by the German National Academic Foundation (Studienstiftung des deutschen Volkes). Günther Raspotnig received financial support from Pro Acarologia Basiliensis (PAB). The synchrotron data was obtained within the BMBF-projects ASTOR and NOVA (05K13VTA, 05K16RDD). Michael Heethoff was supported by the German Research Foundation (HE4593/3–1 and HE4593/5–1). The 700 MHz NMR experiments were performed at the Upper Austrian - South Bohemian Research Infrastructure Center "RERI-uasb" at Johannes Kepler University in Linz, co-financed by the European Union in the context of the project EFRE RU2-EU-124/100–2010 (ETC Austria-Czech Republic 2007–2013, project M00146). We acknowledge support by the German Research Foundation and the Open Access Publishing Fund of Technische Universität Darmstadt. Authors' contributions: Idea and design of the study: MH, GR, AB, SS, RAN; Animal sampling: AB, MH, GR; Collection and analyses of chemical data: AB, GR, MH, SD; Collection and analyses of NMR data: MS, RM, MB; Collection and analysis of morphological data: SS, MH; Predator-prey bioassays: MH, SS; Manuscript drafting: MH, AB, SS, RAN. Equal contributions: MH, AB, SS, MS. All authors read and approved the final manuscript. Availability of data and materials: Morphological data are deposited in MorphDBase repository under accession number: S_Schmelzle_20180122-M-67-001.1 (link: http://www.morphdbase.de/?S_Schmelzle_20180122-M-67.1). The raw chemical data analyzed for the current study are available from the corresponding author upon request. All other materials are attached as supplementary files. Ethics approval: Not applicable. Consent for publication: Not applicable. The authors declare that they have no competing interests.

Attached Files

Published - Heethoff2018_Article_LifeAsAFortressStructureFuncti.pdf

Supplemental Material - 40850_2018_31_MOESM13_ESM.tif

Supplemental Material - 40850_2018_31_MOESM14_ESM.pdf

Supplemental Material - 40850_2018_31_MOESM2_ESM.tif

Supplemental Material - 40850_2018_31_MOESM3_ESM.pdf

Supplemental Material - 40850_2018_31_MOESM4_ESM.tif

Supplemental Material - 40850_2018_31_MOESM5_ESM.tif

Supplemental Material - 40850_2018_31_MOESM6_ESM.tif

Supplemental Material - 40850_2018_31_MOESM7_ESM.tif

Supplemental Material - 40850_2018_31_MOESM8_ESM.tif

Files

40850_2018_31_MOESM14_ESM.pdf
Files (55.1 MB)
Name Size Download all
md5:b75a7afd58e96947cd6f2e8b37a95f8c
22.0 MB Preview Download
md5:70a4dd5c768ad686217e5d70f17b9be2
848.2 kB Preview Download
md5:ed7695e78961f2c583dc51259a146f54
5.2 MB Preview Download
md5:47f13b4a0d42f002026dd9b50dbe199f
909.1 kB Preview Download
md5:099fd79ef0413d7d9749ebee5768d6bf
3.7 MB Preview Download
md5:f294e44672045ce85bd3365828e87e7e
915.9 kB Preview Download
md5:854c563003d221533ff8379b533a1fa0
245.0 kB Preview Download
md5:f36de351bc23ddd0ecb3e9e8245784fd
5.8 MB Preview Download
md5:84f60b70928129db032d0e263832a7e0
1.5 MB Preview Download
md5:b2a26eb5ef94329e3e5aa5c9a32f562b
13.9 MB Preview Download

Additional details

Created:
August 19, 2023
Modified:
October 20, 2023