Abstract
The structural characteristics of silk secretion of the freshwater mite Limnesia maculata (O.F. Müller) (Acariformes, Limnesiidae) are described and analyzed for the first time based on light, atomic force and electron-microscopical approaches. The common dermal glands (14 pairs scattered over the body) produce silk mostly during the warm summer season. The process of silk secretion lasts from several hours to several days. The silk may appear like barely recognized clouds of a fine whitish substance. An individual silk thread is an indefinitely long uniform unbranched and non-stretchable tube, hollow or with a vesicular electron-dense residual content. In the silk bundle, threads may be freely interlaced, bent, curved or occasionally broken. The diameter of the tubes is in the range of 0.9–1.5 µm. The width of the tube walls varies greatly from 60 to 300 nm. Chaotically interlaced fine fibrils build the tube walls. On the external surface of the tube wall, these fibrils are loosely organized and frequently rising vertically, whereas on the internal side they are packed more tightly sometimes showing a mesh. The walls may reveal a layered structure or, contrary, are quite thin with through foramens. The revealed organization of silk in the freshwater mites is found to be the simplest among that of other arthropods. We propose a role of the silk in the capture of potential prey in the summer season. Silk in water mites significantly widens the wholesome area for the mites' life and gives them better chances in competition for potential resources.
Similar content being viewed by others
Data availability
The datasets obtained and analyzed during the current study are available at the Laboratory of Parasitic Arthropods in Zoological Institute of the Russian Academy of Sciences and from the corresponding author on reasonable request.
References
Akai H (1984) The ultrastructure and functions of the silk gland cells of Bombyx mori. In: King RC, Akai H (eds) Insect ultrastructure, vol 2. Plenum Press, New-York, London, pp 323–364
Alberti G, Coons LB (1999) Acari: Mites. In: Harrison FW, Foelix RF (eds) Microscopic anatomy of invertebrates, vol 8C. Wiley, New York, pp 515–1217
Alberti G, Ehrnsberger R, Acari (1977) Rasterelektronenmikroskopische Untersuchungen zum spinnvermögen der Bdelliden und Cunaxiden (Acari, Prostigmata). Acarologia 19:55–61
Annamalai M, Jayaprakash K (2012) Structural studies on silk protein fibre from pseudoscorpion. Int J Life Sci & Pharma Res 2:49–54
Ashton NN, Taggart DS, Stewart RJ (2011) Silk tape nanostructure and silk gland anatomy of Trichoptera. Biopolymers 97:432–445. https://doi.org/10.1002/bip.21720
Bakker De D, Beatens K, Van Nimmen E, Gellynck K, Mertens J, Van Langenhove L, Kiekens P (2006) Description of the structure of different silk threads produced by the water spider Argyroneta aquatica (Clerck, 1757) (Araneae: Cybaeidae). Belg J Zool 136:137–143
Blackledge TA (2013) Spider silk: molecular structure and function in webs. In: Nentwig W (ed) Spider ecophysiology. Springer, Berlin, pp 267–280
Blackledge TA, Scharffb N, Coddingtonc JA, Szütsb T, Wenzeld JW, Hayashie CY, Agnarsson I (2009) Reconstructing web evolution and spider diversification in the molecular era. PNAS 106:5229–5234. https://doi.org/10.1073_pnas.0901377106
Bolland HR (1983) A description of Neophyllobius aesculi n. sp. and its developmental stages (Acari: Camerobiidae). Entomol Ber 43:42–47
Böttger K (1962) Zur Biologie und Ethologie der einheimischen Wassermilben Arrenurus (magaluracarus) globator (Müll.), 1776, Piona nodata nodata (Müll.), 1776, und Eylais infundibulifera meridionalis (Thon), 1899 (Hydrachnellae, Acari). Zool Jahrb System 89:501–584
Büsse S, Hörnschemeye T, Hohu K, McMillan D, Edgerly JS (2015) The spinning apparatus of webspinners – functional-morphology, morphometrics and spinning behavior. Sci Rep 5:9986. https://doi.org/10.1038/srep09986
Clotuche G, Mailleux A-C, Astudillo FA, Deneubourg J-L, Detrain C et al (2011) The formation of collective silk balls in the spider mite Tetranychus urticae Koch. PLoS ONE 6:e18854. https://doi.org/10.1371/journal.pone.0018854
Craig CL (1997) Evolution of arthropod silks. Ann Rev Entomol 42:231–267
Craig CL (2003) Spiderwebs and silk: tracing evolution from molecules to genes to phenotypes. Oxford University Press, Oxford
Craig CL, Riekel C, Herberstein ME, Weber RS, Kaplan D, Pierce NE (2000) Evidence for diet effects on the composition of silk proteins produced by spiders. Mol Biol Evol 17:1904–1913. https://doi.org/10.1093/oxfordjournals.molbev.a026292
Dabert M, Proctor H, Dabert J (2016) Higher-level molecular phylogeny of the water mites (Acariformes: Prostigmata: Parasitengonina: Hydrachnidiae). Mol Phylog Evol 101:75–90. https://doi.org/10.1016/j.ympev.2016.05.004
Engster MS (1976) Studies on silk secretion in the Trichoptera (F. Limnefilidae). I. Histology, histochemistry, and ultrastructure of the silk glands. J Morph 150:183–212
Fernandez AA, Hance T, Clotuche G, Mailleux A-C, Deneubourg JL (2012) Testing for collective choices in the two-spotted spider mite. Exp Appl Acarol 58:11–22. https://doi.org/10.1007/s10493-012-9558-5
Foelix RF (1996) Biology of spiders. Oxford University Press, Oxford
Gerson U (1985) Webbing. In: Helle W, Sabelis MW (eds) Spider mites. Their biology, natural enemies and control, vol 1A. Elsevier, Amsterdam, pp 223–232
Gosline JM, Guerette PA, Ortlepp CS, Savage KN (1999) The mechanical design of spider silks: from fibroin sequence to mechanical function. J Exp Biol 202:3295–3303
Gossel P (1935) Beiträge zur Kenntnis der Hautsinnesorgane und Hautdrüsen der Cheliceraten und der Augen der Ixodiden. Z Morph Ökol Tiere 30:177–205
Gould SA, Tran KT, Spagna JC, Moore AM, Shulman JB (1999) Short and long range order of the morphology of silk from Latrodectus hesperus (Black Widow) as characterized by atomic force microscopy. Int J Biol Macromol 24:151–157
Hajer J, Malý J, Hrubá L, Reháková D (2009) Egg sac silk of Theridiosoma gemmosum (Araneae: Theridiosomatidae). J Morph 270:1269–1283. https://doi.org/10.1002/jmor.10757
Hatano T, Nagashima T (2015) The secretion process of liquid silk with nanopillar structures from Stenopsyche marmorata (Trichoptera: Stenopsychidae). Sci Rep 5:9237. https://doi.org/10.1038/srep09237
Johnson M-L, Merritt DJ, Cribb BW, Trent C, Zalucki MP (2006) Hidden trails: visualizing arthropod silk. Ent Exp Appl 121:271–274. https://doi.org/10.1111/j.1570-8703.2006.00447.x
Kakui K, Hiruta C (2014) Diverse pereopodal secretory systems implicated in thread production in an apseudomorph tanaidacean crustacean. J Morph 275:1041–1052. https://doi.org/10.1002/jmor.20281
Kanazawa M, Sahara K, Saito Y (2011) Silk threads function as an 'adhesive cleaner' for nest space in a social spider mite. Proc Biol Sci 278:1653–1660. https://doi.org/10.1098/rspb.2010.1761
Kerkam K, Viney C, Kaplan D, Lombardi S (1991) Liquid crystallinity of natural silk secretion. Nature 349:596–598
Kirstein K-G, Martin P (2009) Die glandularien der Wassermilben (Hydrachnidia, Acari) – ihre Funktion als Wehrdrüsen. Deutsche Gesellschaft fur Limnologie (DGL). Erweiterte Zusammenfassungen der Jahrestagung 2008 (Konstanz), Hardegsen 2009:571–575
Kirstein K-G, Martin P (2010) Die glandularien der Wassermilben (Hydrachnidia, Acari) – Die Wehrdrüsensekrete im Vergleich. Deutsche Gesellschaft fur Limnologie (DGL). Erweiterte Zusammenfassungen der Jahrestagung 2009 (Oldenburg), Hardegsen 2010:433–437
Knight DP, Vollrath F (2002) Spinning an elastic ribbon of spider silk. Phyl Trans R Soc Lond B 357:219–227.
Kovoor J, Zylberberg L (1980) Fine structural aspects of silk secretion in a spider (Araneus diadematus). I. Elaboration in the pyriform glands. Tissue Cell 12:547–556
Kovoor J, Zylberberg L (1982) Fine structural aspects of silk secretion in a spider. II. Conduction in the pyriform glands. Tissue Cell 14:519–530
Krafft B, Cookson LJ (2012) The role of silk in the behaviour and sociality of spiders. Psyche. https://doi.org/10.1155/2012/529564
Kronenberger K, Moore PG, Halcrow K, Vollrath F (2012) Spinning a marine silk for the purpose of tube-building. J Crustac Biol 32:191–202. https://doi.org/10.1163/193724011X615532
Le Goff GJ, Hance T, Detrain C, Deneubourg J-L, Clotuche G, Mailleux A-C (2011) Impact of starvation on the silk attractiveness in a weaving mite, Tetranychus urticae (Acari: Tetranychidae). J Ethol. https://doi.org/10.1007/s10164-011-0305-x
Li SFY, McGhie AJ, Tang SL (1994) New internal structure of spider dragline silk revealed by atomic force microscopy. Biophys J 66:1209–1212
López–Peña D, Gerecke R, Garcia–Roger EM, Martin P, Jiménez–Peydró R (2022) Parasite–host relationships of water mites (Acari: Hydrachnidia) and black flies (Diptera: Simuliidae) in southeastern Spain. Parasites & Vectors 15:474. https://doi.org/10.1186/s13071-022-05610-2
Lundblad O (1929) Über den Begattungsvorgang bei einigen Arrhenurus-Arten. Z Morphol Ökol Tiere 15:705–722
Manson DCM, Gerson U (1996) Web spinning, wax secretion and liquid secretion by eriophyoid mites. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites – their biology, natural enemies and control. Elsevier, BV, pp 251–258
Miller LD, Putthanarat S, Eby RK, Adams WW (1999) Investigation of the nanofibrillar morphology in silk fibers by small angle X-ray scattering and atomic force microscopy. Int J Biol Macromol 24:159–165
Osborn Popp TM, Addison JB, Jordan JS, Damle VG, Rykaczewski K, Chang SLY, Stokes GY, Edgerly JS, Yarger JL (2016) Surface and wetting properties of embiopteran (webspinner) nanofiber silk. Langmuir 32:4681–4687. https://doi.org/10.1021/acs.langmuir.6b00762
Proctor HC (1991) Courtship in the water mite Neumania papillator: males capitalize on female adaptations for predation. Anim Behav 42:589–598
Proctor HC (1992) Mating and spermatophore morphology of water mites (Acari: Parasitengona). Zool J Linn Soc 106:341–384
Rudall KM, Kenchington W (1971) Arthropod silks: the problem of fibrous proteins in animal tissues. Ann Rev Entomol 16:73–96
Sehnal F, Akai H (1990) Insect silk glands: their type, development and function, and effects of environmental factors and morphogenetic hormones on them. Int J Insect Morphol Embryol 19:79–132
Shatrov AB (2013) Anatomy and ultrastructure of dermal glands in an adult water mite, Teutonia cometes (Koch, 1837) (Acariformes: Hydrachnidia: Teutoniidae). Arthr Str Dev 42:115–125. https://doi.org/10.1016/j.asd.2012.10.006
Shatrov AB, Soldatenko EV (2016) Dermal glands in freshwater mites Limnesia undulata (O.F. Müller, 1776) and L. fulgida (C.L. Koch, 1836) (Acariformes, Limnesiidae). Arthr Str Dev 45:341–355. https://doi.org/10.1016/j.asd.2016.05.003
Shatrov AB, Soldatenko EV (2022) Organization of dermal glands and characteristic of secretion in the freshwater mite, Limnesia maculata (O.F. Muller, 1776) (Acariformes, Limnesiidae). J Morph 283:346–362.
Shatrov AB, Soldatenko EV, Gavrilova OV (2014) Observation on silk production and morphology of silk in water mites (Acariformes: Hydrachnidia). Acarina 22:133–148
Shatrov AB, Soldatenko EV, Gavrilova OV (2016) Morphology of tube-like threads related to Limnochares aquatica (L., 1758) (Acariformes: Hydrachnidia: Limnocharidae) in the laboratory. J Nat Hist 50:2199–2214. https://doi.org/10.1080/00222933.2016.1193643
Shatrov AB, Soldatenko EV, Stolbov VA, Smirnov PA, Petukhova OA (2019) Ultrastructure and functional morphology of dermal glands in the freshwater mite Limnochares aquatica (L., 1758) (Acariformes, Limnocharidae). Arthr Str Dev 49:85–102. https://doi.org/10.1016/j.asd.2018.11.010
Smith BP, Hagman J (2002) Experimental evidence for a female sex pheromone in Arrenurus manubriator (Acari: Hydrachnida; Arrenuridae). Exp Appl Acarol 27:257–263. https://doi.org/10.1023/a:1023328428716
Sokolov II (1940) Faune de l’URSS. Arachnides. Vol. V. Issue 2. Hydracarina (1-re partie: Hydrachnellae). Edition de l’Academie des Sciences de l’URSS, Moscou, Leningrad. [In Russian]
Sponner A, Vater W et al (2007) Composition and hierarchical organisation of a spider silk. PLoS ONE 2:e998. https://doi.org/10.1371/journal.pone.0000998
Sponner A, Schlott B, Vollrath F, Unger E, Grosse F, Weisshart K (2005) Characterization of the protein components of Nephila clavipes dragline silk. Biochemistry 44:4727–4736. https://doi.org/10.1021/bi047671k
Stubbs DG, Tillinghast EK, Townley MA (1992) Fibrous composite structure in a spider silk. Naturwissenschaften 79:231–234
Sutherland TD, Young JH, Weisman S, Hayashi CY, Merritt DJ (2010) Insect silk: one name, many materials. Ann Rev Entomol 55:171–188. https://doi.org/10.1146/annurev-ento-112408-085401
Tsalolokhin SJ (ed) (1997) Key to freshwater invertebrates of Russia and adjacent lands. T. 3. Arachnida, lower Insects. Zoological Institute of the Russian academy of Sciences, St.-Petersburg
Vasquez AA, Mohiddin O, Li Z, Bonnici BL, Gurdziel K, Ram JL (2021) Molecular diet studies of water mites reveal prey biodiversity. PLoS ONE 16:e0254598. https://doi.org/10.1371/journal.pone.0254598
Vasquez AA, Bonnici BL, Yusuf SH, Cruz JI, Hudson PL, Ram JL (2022) Improved Chironomid barcode database enhances identification of water mite dietary content. Diversity. https://doi.org/10.3390/d14020065
Vollrath F (2000) Strength and structure of spiders’ silks. Rev Mol Biotech 74:67–83. https://doi.org/10.1016/s1389-0352(00)00006-4
Vollrath F, Knight DP (2001) Liquid crystalline spinning of spider silk. Nature 410:541–548. https://doi.org/10.1038/35069000
Vollrath F, Holtet T, Thøgersen HC, Frische S (1996) Structural organization of spider silk. Proc R Soc Lond B 263:147–151
Wallace MMH, Mahon JA (1972) The taxonomy and biology of Australian Bdellidae (Acari). I. Subfamilies Bdellinae, Spinibdellinae and Cytinae. Acarologia 14:544–580
Wiles PR (1997) The homology of glands and glandularia in the water mites (Acari: Hydrachnidia). J Nat Hist 31:1237–1251
Witte H (1991) Indirect sperm transfer in prostigmatic mites from a phylogenetic viewpoint. In: Schuster R, Murphy PW (eds) The Acari: Reproduction, Development and life history strategies. Chapman & Hall, London, pp 173–178
Witte H, Döring D (1999) Canalized pathways of change and constraints in the evolution of reproductive modes of microarthropods. Exp Appl Acarol 23:181–216
Yano S (2012) Cooperative web sharing against predators promotes group living in spider mites. Behav Ecol Soc. Available from: http://hdl.handle.net/2433/153051
Yonemura N, Sehnal F, Mita K, Tamura T (2006) Protein composition of silk filaments spun under water by caddisfly larvae. Boimacromolecules 7:3370–3378. https://doi.org/10.1021/bm060663u
Young JH, Merritt DJ (2003) The ultrastructure and function of the silk-producing basitarsus in the Hilarini (Diptera: Empididae). Arthr Str Dev 32:157–165. https://doi.org/10.1016/S1467-8039(03)00006-9
Acknowledgements
This study is undertaken and performed under the State Government Research Programs ## 122031100263-1, 122031100275-4 and 122031100281-5. The TEM, SEM and CLSM procedures were completed using the Core Facilities Centre ‘Taxon’ at the Zoological Institute of the Russian Academy of Sciences (St. Petersburg, Russia, https://www.ckp-rf.ru/ckp/3038/). The AFM methods were performed in the Centre for Microscopy and Microanalysis (St. Petersburg State University, St. Petersburg, Russia). We thank to Dr. S.V. Shabelnikov (Institute of Cytology Russian Academy of Sciences, St. Petersburg, Russia) for his assistance and consultations on the spectroscopic methods.
Funding
This work was supported by the State Government Research Programs ## 122031100263-1 (A.B. Shatrov), 122031100275-4 (E.V. Soldatenko) and 122031100281-5 (A.A. Petrov).
Author information
Authors and Affiliations
Contributions
AS performed the experiments, wrote the main manuscript text and prepared figures, ES kept mites in laboratory culture, KB performed AFM processing, AP performed confocal laser processing, All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Competing interest
The authors declare no competing interest.
Ethical approval
This is an observational study. No ethical approval is required.
Consent for participant
Informed consent was obtained from all individual participants included in the study.
Consent to publication
of the scientific figures and videos and individual contact data has been received from all participants of this work.
Additional information
Publisher’s Note
Springer nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Supplementary material 1 (MP4 4083.4 kb)
Supplementary material 2 (MP4 4929.7 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Shatrov, A.B., Soldatenko, E.V., Benken, K.A. et al. The structural analysis of secretion in the freshwater mite Limnesia maculata (Acariformes, Limnesiidae) supports the idea of a new form of arthropod silk. Exp Appl Acarol 90, 277–300 (2023). https://doi.org/10.1007/s10493-023-00826-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-023-00826-y