Skip to main content

Chemical basis of unwettability in Liacaridae (Acari, Oribatida): specific variations of a cuticular acid/ester-based system

Abstract

Oribatid mites of the family Liacaridae comprise a large number of species with smooth and shiny body surfaces that display extraordinary anti-wetting properties. The principle of liacarid unwettability is not related to micro-structured surfaces as present in many Oribatida (“Lotus effect”) but the formation of raincoat-like lipid layers covering the epicuticle. We here conducted a comparative study on the chemistry of cuticular lipid layers in a selection of Liacaridae, including representatives of all major Central European genera, Liacarus, Dorycranosus, Adoristes, and Xenillus. Cuticular lipids of unwettable individuals were removed from mite bodies by hexane extraction, and were analyzed by GC–MS. Basically, two chemically distinguishable systems were found. Type I: cuticular lipids of Liacarus subterraneus, L. coracinus, L. nitens, Dorycranosus curtipilis, and Xenillus tegeocranus contained different carboxylic acids (C8-, C10-, C10:1-, C10:2-acids) and their corresponding di-glycerides in species-specific combinations. Type II: Adoristes ovatus exhibited a system of cuticular lipids composed of esters of pentanoic- and heptanoic acids with C14-, C15-, C16- and C17-alcohols. Interestingly, the chemistry of surface lipids did not reflect the morphology of the cuticle in the species investigated. Smooth and shiny cuticles, though exhibiting a specific pattern of round or slit-like pores, were found in representatives of Liacarus, Dorycranosus (all of which exhibiting cuticular chemistry of type I) and Adoristes (exhibiting cuticular chemistry of type II). Xenillus, possessing a rough, cerotegumental cement layer-covered surface, showed type I-chemistry. The acid–esters systems herein investigated are considered characteristic for the cuticular chemistry of Liacaridae or a lineage of these, and provide first insights into the comparative chemistry of the inner (=lipid) layer of the oribatid cerotegument.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. A’Bear AD, Boddy L, Raspotnig G, Jones TJ (2010) Non-trophic effects of oribatid mites on cord-forming basidiomycetes in soil microsoms. Ecol Entomol 35:477–484. doi:10.1111/j.1365-2311.2010.01204.x

    Google Scholar 

  2. Alberti G, Storch V, Renner H (1981) Über den feinstrukturellen Aufbau der Milbencuticula (Acari: Arachnida). Zool Jahrb Abt Anat Ontog Tiere 105:183–236

  3. Alberti G, Norton RA, Adis J, Fernandez NA, Kratzmann M, Moreno A, Ribiero E, Weigmann G, Woas S (1997) Porose integumental organs of oribatid mites (Acari, Oribatida). 2. Fine structure. Zoologica (Stuttgart) 146:33–114

    Google Scholar 

  4. Belsito EL, Carbone C, Di Gioia ML, Leggio A, Liguoiri A, Perri F, Siciliano C, Viscomi MC (2007) Comparison of the volatile constituents in cold-pressed bergamot oil and a volatile oil isolated by vacuum distillation. J Agric Food Chem 55:7847–7851. doi:10.1021/jf070997q

    CAS  PubMed  Google Scholar 

  5. Blomquist GJ, Dillwith JW (1985) Cuticular lipids. In: Kerkut GA, Gilbert LJ (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 3. Pergamon Press, Oxford, pp 117–154

    Google Scholar 

  6. Bou DD, Lago JH, Figueiredo CR, Matsuo AL, Guadagnin RC, Soares MG, Sartorelli P (2013) Chemical composition and cytotoxicity evaluation of essential oil from leaves of Casearia sylvestris, its main compound α-zingiberene and derivatives. Molecules 18:9477–9487. doi:10.3390/molecules18089477

    Article  CAS  PubMed  Google Scholar 

  7. DeRenobales M, Nelson DR, Blomquist GJ (1991) Cuticular lipids. In: Binnington K, Retnakaran A (eds) Physiology of the insect epidermis. CSIRO Publications, Australia, pp 240–251

    Google Scholar 

  8. Erdmann G, Otte V, Langel R, Scheu S, Maraun M (2007) The trophic structure of bark-living oribatid mite communities analysed with stable isotopes ((15)N, (13)C) indicates strong niche differentiation. Exp Appl Acarol 41:1–10. doi:10.1007/s10493-007-9060-7

    PubMed  Google Scholar 

  9. Flamini G, Luigi Cioni P, Morelli I, Celik S, Gokturk RS, Unal O (2005) Essential oil of Stachys aleurites from Turkey. Biochem Syst Ecol 33:61–66. doi:10.1016/j.bse.2004.05.013

    CAS  Google Scholar 

  10. Glenn DM, Puterka GJ, van der Zwet T, Byers RE, Feldhake C (1999) Hydrophobic particle films: a new paradigm for suppression of arthropod pests and plant diseases. J Econ Entomol 92:759–771

    Google Scholar 

  11. Heethoff M (2012) Regeneration of complex oil-gland secretions and its importance for chemical defense in an oribatid mite. J Chem Ecol 38:1116–1123. doi:10.1007/s10886-012-0169-8

    CAS  PubMed  Google Scholar 

  12. Heethoff M, Rall BC (2015) Reducible defense: chemical protection alters the dynamics of predator-prey interactions. Chemoecology 25:53–61. doi:10.1007/s00049-014-0184-z

    Article  Google Scholar 

  13. Heethoff M, Koerner L, Norton RA, Raspotnig G (2011) Tasty but protected—first evidence of chemical defense in oribatid mites. J Chem Ecol 37:1037–1043. doi:10.1007/s10886-011-0009-2

    CAS  PubMed  Google Scholar 

  14. Helbig R, Nickerl J, Neinhuis C, Werner C (2011) Smart skin patterns protect springtails. PLoS One 6(9):e25105. doi:10.1371/journal.pone.0025105

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Hinton HE (1960) How some insects, especially the egg stages, avoid drowning when it rains. J Insect Physiol 4:138–154

    Google Scholar 

  16. Ito N, Wada S, Yamanaka Y, Takagaki H, Nakamura H (2005) Identification of novel decenoic acids in heated butter. Biosci Biotechnol Biochem 69:2416–2420. doi:10.1271/bbb.69.2416

    CAS  PubMed  Google Scholar 

  17. Jackson LL, Baker GL (1970) Cuticular lipids of insects. Lipids 5:239–246. doi:10.1007/BF02532475

    Article  CAS  Google Scholar 

  18. Jackson LL, Blomquist GF (1976) Insect waxes. In: Kolattukudy PE (ed) Chemistry and biochemistry of natural waxes. Elsevier, Amsterdam, pp 201–233

    Google Scholar 

  19. Johnson RH, Hull-Sanders HM, Meyer GA (2007) Comparison of foliar terpenes between native and invasive Solidago gigantean. Biochem Syst Ecol 35:821–830. doi:10.1016/j.bse.2007.06.005

    CAS  Google Scholar 

  20. Kawana S, Nakagawa K, Hesegawa Y, Kobayashi H, Yamaguchi S (2008) Improvement of sample throghput using gas chromatography–mass spectrometry for biochemical diagnosis of organic acid disorders. Clin Chim Acta 392(1–2):34–40. doi:10.1016/j.cca.2008.02.025

    CAS  PubMed  Google Scholar 

  21. Kerstiens G (2001) Plant Cuticle. In: Roberts K (ed) Handbook of plant science, vol 1. Wiley, New York, pp 151–153

    Google Scholar 

  22. Khalilov LM, Khalilova AZ, Odinokov VN, Baltaev UA, Paramonov EA, Dzhemilev UM (1999) Identification and biological activity of the volatile organic substances emitted by plants and insects—II. Sesquiterpene composition of the native scent of leaves of the potato Solanum tuberosum. Chem Nat Compd 35:422–426. doi:10.1007/2FBF02282508

    CAS  Google Scholar 

  23. Khalilova AZ, Paramonov EA, Odinokov VN, Khalilov LM (1998) Identification and biological activity of volatile organic substances emitted by plants and insects. I. Components of the native scents of Leptinotarsa decemlineata and Solanum tuberosum. Chem Nat Compd 34:647–649. doi:10.1007/BF02319296

    CAS  Google Scholar 

  24. Kuwahara Y, Leal WS, Nakano Y, Kaneko Y, Nakao H, Suzuki T (1989) Pheromone study on astigmatid mites XXIII. Identification of the alarm pheromone on the acarid mite, Tyrophagus neiswanderi and species specificities of alarm pheromones among four species of the same genus. Appl Entomol Zool 24:424–429

    CAS  Google Scholar 

  25. Kuwahara Y, Ohshima M, Sato M, Kurosa K, Matsuyama S, Suzuki T (1995) Chemical ecology of astigmatid mites XL. Identification of the alarm pheromone and new C17 hydrocarbons from Tortonia sp., a pest attacking the nest of Osmia cornifrons. Appl Entomol Zool 30:177–184

    CAS  Google Scholar 

  26. Lazarus S, Krisper G (2014) Diversity of the oribatid mite fauna (Acari, Oribatida) in two dry meadows in Styria (Austria). Soil Org 86:117–124

    Google Scholar 

  27. Leis HJ, Fauler G, Windischofer W (2014) Enantioselective quantitative analysis of amphetamine in human plasma by liquid chromatography/high-resolution mass spectrometry. Anal Bioanal Chem 406:4473–4480. doi:10.1007/s00216-014-7850-4

    CAS  PubMed  Google Scholar 

  28. Lockey KH (1988) Lipids of the insect cuticle: origin, composition and function. Comp Biochem Physiol 81 B:223–227. doi:10.1016/0305-0491(88)90305-7

    Google Scholar 

  29. Maraun M, Scheu S (2000) The structure of oribatid mite communities (Acari, Oribatida): patterns, mechanisms and implications for future research. Ecography 23:374–383. doi:10.1111/j.1600-0587.2000.tb00294.x

    Article  Google Scholar 

  30. Maraun M, Erdmann G, Schulz G, Norton RA, Scheu S, Domes K (2009) Multiple convergent evolution of arboreal life in oribatid mites indicates the primacy of ecology. Proc R Soc B 276:3219–3227. doi:10.1098/rspb.2009.0425

    PubMed Central  CAS  PubMed  Google Scholar 

  31. Marcell LM, Beattie GA (2002) The effect of leaf surface waxes on leaf colonization by Pantoea agglomerans and Clavibacter michiganensis. Mol Plant-Microbe Interact 15:1236–1244. doi:10.1094/MPMI.2002.15.12.1236

    CAS  PubMed  Google Scholar 

  32. Mevy JP, Bessiere JM, Greff S, Zombre G, Viano J (2006) Composition of the volatile oil from the leaves of Ximenia americana L. Biochem Syst Ecol 34:549–553. doi:10.1016/j.bse.2006.01.007

    CAS  Google Scholar 

  33. Neinhuis C, Barthlott W (1997) Characterisation and distribution of water-repellent. Self-cleaning plant surfaces. Ann Bot 79:667–677. doi:10.1006/anbo.1997.0400

    Google Scholar 

  34. Pitarokili D, Tzakou O, Loukis A, Harvala C (2003) Volatile metabolites from Salvia fruticosa as antifungal agents in soilborne pathogens. J Agric Food Chem 51:3294–3301. doi:10.1021/jf0211534

    CAS  PubMed  Google Scholar 

  35. Rasband WS (1997–2014) ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/. Accessed 29 December 2014

  36. Raspotnig G (2006) Chemical alarm and defense in the oribatid mite Collohmannia gigantea (Acari: Oribatida). Exp Appl Acarol 39:177–194. doi:10.1007/s10493-006-9015-4

    CAS  PubMed  Google Scholar 

  37. Raspotnig G (2010) Oil gland secretions in Oribatida (Acari). In: Sabelis MW, Bruin J (eds) Trends in acarology. Springer, Dordrecht, pp 235–239. doi:10.1007/978-90-481-9837-5_38

    Google Scholar 

  38. Raspotnig G, Krisper G (1998) Fatty acids as cuticular surface components in oribatid mites (Acari: Oribatida). Biosyst Ecol Ser 14: 215–243. In: Ebermann E (ed) Arthropod biology: contributions to morphology, ecology, and systematics. Austrian Academy of Sciences, Vienna

  39. Raspotnig G, Leis H-J (2009) Wearing a raincoat: exocrine secretions contain anti-wetting agents in the oribatid mite, Liacarus subterraneus (Acari: Oribatida). Exp Appl Acarol 47:179–190. doi:10.1007/s10493-008-9212-4

    CAS  PubMed  Google Scholar 

  40. Raspotnig G, Matischek T (2010) Anti-wetting strategies of soil-dwelling Oribatida. Acta Soc Zool Bohem 74:91–96

    Google Scholar 

  41. Raspotnig G, Kaiser R, Stabentheiner E, Leis H-J (2008a) Chrysomelidial in the opisthonotal glands of the oribatid mite, Oribotritia berlesei. J Chem Ecol 34:1081–1088. doi:10.1007/s10886-008-9508-1

    PubMed Central  CAS  PubMed  Google Scholar 

  42. Raspotnig G, Krisper G, Fauler G, Leis H-J (2008b) Distinctive cuticular hydrocarbon profiles in oribatid mites (Acari: Oribatida). Ann Zool (Warszawa) 58:445–452

    Google Scholar 

  43. Sakata T, Tagami K, Kuwahara Y (1995) Chemical ecology of oribatid mites. I. Oil gland components of Hydronothrus crispus Aoki. J Acarol Soc Jpn 4:69–75

    Google Scholar 

  44. Schatz H (2002) Die Oribatidenliteratur und die beschriebenen Oribatidenarten (1758–2001)—eine analyse. Abh Ber Nat Mus Görlitz 74:37–45

    Google Scholar 

  45. Schatz H, Schatz I, Pfaller K, Salvenmoser W (2006) Cuticuläre Feinstrukturen der Hornmilbe Xenillus athesis Schatz, 2004 (Acari, Oribatida), einer neuen Tierart aus Südtirol (Prov. Bozen, Italien). Gredleriana 6:395–400

    Google Scholar 

  46. Schneider K, Migge S, Norton RA, Scheu S, Langel R, Reineking A, Maraun M (2004) Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15 N/14 N). Soil Biol Biochem 36:1769–1774. doi:10.1016/j.soilbio.2004.04.033

    CAS  Google Scholar 

  47. Sharma KR, Seenivasagan T, Rao AN, Ganesan K, Agrawal OP, Malhotra RC, Prakash S (2008) Oviposition responses of Aedes aegypti and Aedes albopictus to certain fatty acid esters. Parasitol Res 103:1065–1073. doi:10.1007/s00436-008-1094-1

    PubMed  Google Scholar 

  48. Shimizu N, Noge K, Mori N, Nishida R, Kuwahara Y (2004) Chemical ecology of astigmatid mites LXXIII. Neral as an alarm pheromone of the acarid mite, Oulenzia sp. (Astigmata: Winterschmidtiidae). J Acarol Soc Jpn 13:57–64. doi:10.2300/acari.13.57

    Google Scholar 

  49. Subias LS (2004, onwards) Listado sistimatico, sininimico y biogeografico de los Acaros Oribatidos (Acariformes, Oribatida) del mundo. Graellsia 60:3–305

    Article  Google Scholar 

  50. Taiz L, Zeiger E (2010) Plant physiology. Sinauer Associates, Sunderland

    Google Scholar 

  51. Tretyakov KV (2007) Retention data. NIST mass spectrometry data center. http://webbook.nist.gov/cgi/inchi/InChI%3D1S/C13H26O2Si/c1-5-6-7-8-9-10-11-12-13%2814%291516%282,3%294/h5H,1,6-12H2,2-4H3. Accessed 29 December 2014

  52. Van Den Dool H, Kratz PD (1963) A generalization of the retention index system including linear temperature programmed gas—liquid partition chromatography. J Chromatography 11:463–471. doi:10.1016/S0021-9673(01)80947-X

    Google Scholar 

  53. Weigmann G (2006) Hornmilben (Oribatida). Goecke and Evers, Keltern

    Google Scholar 

  54. Woolley TA (1967) North American Liacaridae, I—Adoristes and a related new genus. J Kansas Entomol Soc 40:270–276

    Google Scholar 

  55. Woolley TA (1968) North American Liacaridae, II—Liacarus (Acari: Cryptostigmata). J Kansas Entomol Soc 41:350–366

    Google Scholar 

  56. Woolley TA (1969) North American Liacaridae, III—New genera and species. J Kansas Entomol Soc 42:183–194

    Google Scholar 

  57. Woolley TA, Higgins HG (1966) Xenillidae, a new family of oribatid mites (Acari: Cryptostigmata). J NY Entomol Soc 74:201–221

    Google Scholar 

  58. Young AM, Blum MS, Fales HM, Bian Z (1986) Natural history and ecological chemistry of the neotropical butterfly Papilio anchisiades papilionidae. J Lepidop Soc 40:36–53

    Google Scholar 

Download references

Acknowledgments

A.K.B. was supported by a short-term grant provided by the German National Academic Foundation (Studienstiftung des deutschen Volkes) which also founded his trip to Finland as a part of “Expedition Academy 2014: Mariehamn”. G.R. received financial support from Pro Acarologia Basiliensis (PAB). We thank Michaela Bodner (Institute of Zoology, University of Graz, Austria), Petra Föttinger (Graz and Paracelsus Medical University in Salzburg, Austria), Kathrin Kuess (Graz, Austria) and Oana Lusco (Graz, Austria) for providing specimens from Austria, Romania and Spain. We are thankful to Katja Domes-Wehner (Ecological Networks, Department of Biology, Darmstadt University of Technology, Germany) for providing some phylogenetic information on Liacaridae and related families. Furthermore, we want to express our gratitude to Alexander Schießer (MS-Section, Department of Chemistry, Darmstadt University of Technology, Germany) for HRMS-measurements and some advice on compound identification. We are grateful to Günther Krisper (Institute of Zoology, University of Graz) for his advice to find probable collection localities and his help with the determination of different Licaridae species. We are thankful to Michael Heethoff and Sebastian Schmelzle (both, Ecological Networks, Department of Biology, Darmstadt University of Technology, Germany) for critically reading the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Günther Raspotnig.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Brückner, A., Stabentheiner, E., Leis, HJ. et al. Chemical basis of unwettability in Liacaridae (Acari, Oribatida): specific variations of a cuticular acid/ester-based system. Exp Appl Acarol 66, 313–335 (2015). https://doi.org/10.1007/s10493-015-9914-3

Download citation

Keywords

  • Liacarus
  • Dorycranosus
  • Adoristes
  • Xenillus
  • Water repellency
  • Raincoat
  • Cerotegument
  • Cuticular chemistry
  • Lipid layer