Abstract
Although the phylum Gastrotricha is known and studied for more than 150 years, some cell types, tissues and organ systems are still not well understood in terms of their morphology, ultrastructure, function and role. One of these features is the epidermal gland system (EGS). As yet, there is just a single detailed electron microscopic investigation of the epidermal glands of the species Turbanella cornuta Remane, 1925, plus scattered ultrastructural data of few additional species. We comprehensively investigated the epidermal glands of Tetranchyroderma suecicum Boaden, 1960 by means of serial sectioning and transmission electron microscopy (TEM) and with scanning electron microscopy. Furthermore, light microscopical, confocal laser scanning microscopical and micro-computed tomographical (µCT) techniques were additionally used for this investigation. Computer programs for 3D-reconstructions were used to analyse the data obtained by TEM and µCT. Tetranchyroderma suecicum possesses up to 100, mostly pairwise arranged, glandulocytes. Each single-celled gland contains a large anastomosing secretory cistern with granular content, has a very electron-dense cytoplasm, a basally positioned nucleus, peripherally arranged mitochondria and a cuticulated, ‘chimney-like’ apical neck, which carries the cellular pore. Each merocrine glandulocyte is associated with an adjacent ciliated sensory cell. There is currently no coherent hypothesis of the glandulocytes’ functional role, but different ideas are discussed. We refer to evidence that the secretory product of the EGS of Tetranchyroderma suecicum most likely acts as a repellent against potential predators.
Similar content being viewed by others
References
Angermüller S, Fahimi HD (1982) Imidazole-buffered osmium tetroxide: an excellent stain for visualization of lipids in transmission electron microscopy. Histochem J 14:823–835
Balsamo M, Grilli P, Guidi L, d’Hondt J-L (2014) Gastrotricha: biology, ecology and systematics: families Dasydytidae, Dichaeturidae, Neogosseidae, Proichthydiidae. Identification Guides to the Plankton and Benthos of Inland Waters, vol 24. Backuys Publishers, Margraf Publishers, Weikersheim
Belazi D, Solé-Domènech S, Johansson B, Schalling M, Sjövall P (2009) Chemical analysis of osmium tetroxide staining in adipose tissue using imaging ToF-SIMS. Histochem Cell Biol 132:105–115
Boaden PJS (1960) Three new Gastrotrichs from the Swedish west coast. Cahr Biol Mar 1:397–406
Cerca J, Purschke G, Struck HG (2018) Marine connectivity dynamics: clarifying cosmopolitan distributions of marine interstitial invertebrates and the meiofauna paradox. Mar Biol 165:123
Chute CD, Srinivasan J (2014) Chemical mating cues in C. elegans. Semin Cell Dev Biol 33:18–24
Giere O (2009) Gastrotricha. In: Giere O (ed) Meiobenthology—the microscopic motile fauna of aquatic sediments, 2nd edn. Springer, Berlin, pp 162–164
Greenspan P, Mayer EP, Fowler SD (1985) Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100:965–973
Groseclose MR, Massion PP, Chaurand P, Caprioli RM (2008) High-throughput proteomic analysis of formalin-fixed paraffin-embedded tissue microarrays using MALDI imaging mass spectrometry. Proteomics 8(18):3715–3724
Harwood JL (1988) Fatty acid metabolism. Ann Rev Plant Physiol Plant Mol Biol 39:101–138
Higgins RP, Thiel H (1988) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, p 488
Hochberg R (2010a) Two new species of Oregodasys (Gastrotricha: Macrodasyida: Thaumastodermatidae) from Carrie Bow Cay, Belize with ultrastructural observations of the epidermal glandular system. Zootaxa 2660:1–17
Hochberg R (2010b) The epidermal glands of gastrotrichs: ultrastructural insights and hypotheses of function. Integr Comp Biol 50:e76
Hochberg R, Atherton S (2011) A new species of Lepidodasys (Gastrotricha, Macrodasyida) from Panama with a description of its peptidergic nervous system using CLSM, anti-FMRFamide anti-SCPB. Zoologischer Anzeiger 250:111–122
Holtmann M, Thurm U (2001) Mono-and oligo-vesicular synapses and their connectivity in a Cnidarian sensory epithelium (Coryne tubulosa). J Comp Neurol 432(4):537–549
Kieneke A, Nikoukar H (2017) Integrative morphological and molecular investigation of Turbanella hyalina Schultze, 1853 (gastrotricha: Macrodasyida), including a redescription of the species. Zoologischer Anzeiger 267:168–186
Kieneke A, Schmidt-Rhaesa A (2015) Gastrotricha. In: Schmidt-Rhaesa A (ed) Handbook of zoology. Gastrotricha, Cycloneuralia and Gnathifera. Gastrotricha and Gnathifera, vol 3. De Gruyter, Berlin, p 134
Kieneke A, Riemann O, Ahlrichs WH (2008) Novel implications for the basal internal relationships of Gastrotricha revealed by an analysis of morphological characters. Zool Scr 37:429–460
Kieneke A, Schmidt-Rhaesa A, Hochberg R (2015) A new species of Cephalodasys (Gastrotricha, Macrodasyida) from the Caribbean Sea with a determination key to species of the genus. Zootaxa 3947:367–385
Kompauer M, Heiles S, Spengler B (2017) Atmospheric pressure MALDI mass spectrometry imaging of tissues and cells at 1.4 µm lateral resolution. Nat Methods 14:90–96. https://doi.org/10.1038/nmeth.4071
Lee J, Chang CY (2011) Two new species of the genus Lepidodasys (Gastrotricha, Lepidodasyidae) from Tsushima Island, Japan. J Nat Hist 45:855–867
Lehninger AL (1985) Grundkurs Biochemie. Translated by Neubert, D. & Hucho, F. De Gruyter, Berlin, p 515
Leighton DHW, Sternberg PW (2016) Mating pheromones of Nematoda: olfactory signaling with physiological consequences. Curr Opin Neurobiol 38:119–124
Metscher BD (2009) MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol 9:11. https://doi.org/10.1186/1472-6793-9-11
Mulisch M, Welsch U (eds) (2010) Romeis Mikroskopische Technik. Spektrum Akademischer Verlag, Heidelberg, p 551
Münter L, Kieneke A (2017) Novel myo-anatomical insights to the Xenotrichula intermedia species complex (Gastrotricha: Paucitubulatina): implications for a pan-European species and reconsideration of muscle homology among Paucitubulatina. Proc Biol Soc Wash 130:165–185
Pfannkuche O, Thiel H (1988) Sample processing. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 134–145
Rieder N, Schmidt K (1987) Morphologische Arbeitsmethoden in der Biologie. VCH Verlagsgesellschaft, Weinheim, p 223
Rieger GE, Rieger RM (1977) Comparative fine structure study of the Gastrotrich cuticle ans aspects of cuticle evolution within the Aschelminthes. Zeitschrift für zoologische Systematik und Evolutionsforschung 15:81–124
Rieger RM, Ruppert E, Rieger GE, Schoepfer-Sterrer C (1974) On the fine structure of gastrotrichs with description of Chordodasys antennatus sp n. Zool Scr 3:219–237
Röhl I, Schneider B, Schmidt B, Zeeck E (1999) L-Ovothiol A: the egg release pheromone of the marine Polychaete Platynereis dumerilii: Annelida: Polychaeta. Z Naturforsch 54:1145–1147
Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET, Eliceiri KW (2017) Image J2: ImageJ for the next generation of scientific image data. BMC Bioinform 18:529. https://doi.org/10.1186/s12859-017-1934-z
Ruppert EE (1991) Gastrotricha. In: Harrison FH, Ruppert EE (eds) Microscopic anatomy of invertebrates, vol 4. Wiley-Liss, New York, pp 41–109
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9(7):676–682. https://doi.org/10.1038/nmeth.2019
Schuster J, Atherton S, Todaro MA, Schmidt-Rhaesa A, Hochberg R (2018) Redescription of Xenodasys riedli (Gastrotricha: Macrodasyida) based on SEM analysis, with first report of population density data. Mar Biodivers 48:259–271
Stanley-Samuelson DW, Jurenka RA, Cripps C, Blomquist GJ, de Renobales M (1988) Fatty acids in insects: composition, metabolism, and biological significance. Arch Insect Biochem Physiol 9:1–33
Storch V, Welsch U (2004) Kurzes Lehrbuch der Zoologie. Springer, Berlin, p 672
Suzuki T, Fujikura K, Higashiyama T, Takata K (1997) DNA staining for fluorescence and laser confocal microscopy. J Histochem Cytochem 45(1):49–53
Teuchert G (1977) The ultrastructure of the marine Gastrotrich Turbanella cornuta Remane (Macrodasyoidea) and its functional and phylogenetical importance. Zoomorphologie 88:189–246
Todaro MA (2002) An interesting new gastrotrich from littoral meiobenthos (Long Beach Island, USA), with a key to species of Tetranchyroderma (Gastrotricha: Macrodasyida). J Mar Biol Ass UK 82:555–563
Todaro MA, Hummon WD (2008) An overview and a dichotomous key to genera of the phylum Gastrotricha. Meiofauna Marina 16:3–20
Todaro MA, Sibaja-Cordero JA, Segura-Bermúdez OA, Coto-Delgado G, Goebel-Otárola N, Barquero JD, Cullell-Delgado M, Dal Zotto M (2019) An introduction to the study of Gastrotricha, with a taxonomic key to families and genera of the group. Diversity 2019(11):117
Tomaschko K-H (1994) Ecdysteroids from Pycnogonum litorale (Arthropoda, Pantopoda) act as a chemical defense against Carcinus maenas (Crustacea, Decapoda). J Chem Ecol 20(7):1445–1455
Tyler S, Rieger GE (1980) Adhesive organs of the Gastrotricha I. Duo-gland organs. Zoomorphologie 95:1–15
Tyler S, Melanson LA, Rieger RM (1980) Adhesive organs of the Gastrotricha II. The Organs of Neodasys. Zoomorphologie 95:17–26
Ude J, Koch M (2002) Die Zelle: Atlas der Ultrastruktur. Spektrum Akademischer Verlag, Heidelberg, pp 1–328
Westfall JA, Elliott CF, Carlin RW (2002) Ultrastructural evidence for two-cell and three-cell neural pathways in the tentacle epidermis of the sea anemone Aiptasia pallida. J Morphol 251:83–92
Wulf E, Deboben A, Bautz FA, Faulstich H, Wieland T (1979) Fluorescent phallotoxin, a tool for the visualization of cellular actin. Proc Natl Acad Sci USA 76(9):4498–4502
Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31(3):1116–1128
Acknowledgements
Sincere thanks are given to Björn M. von Reumont and to Alexander Blanke for preparing and hosting the workshop “From synchrotron based micro-CT scans to 3D models and beyond” (May 2017). Many thanks also to Jannis Ortgies, who patiently prepared many of the TEM slices used for the current study. Furthermore, we acknowledge the Forschen@Studium Grant of the Carl von Ossietzky University Oldenburg (program Forschungsbasiertes Lernen im Fokus plus, FliF +), which allowed us to present the results of this study at the 17th International Meiofauna Conference in Évora, Portugal (July 2019). The µCT facility at the FAU was supported by a Grant of the German Science Foundation (DFG funding no. 274877207). The comments and modifications provided by two anonymous reviewers significantly improved our manuscript, many thanks to them. This is publication number 47 that uses data from the Senckenberg am Meer Confocal Laserscanning Microscope Facility.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and institutional guidelines for the care and use of animals were followed. No endangered species or animals from protected areas were used for this study. This article does not contain any studies with human participants performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Schnier, J., Ahlrichs, W.H., Gruhl, A. et al. Ultrastructure of the epidermal gland system of Tetranchyroderma suecicum Boaden, 1960 (Gastrotricha: Macrodasyida) indicates a defensive function of its exudate. Zoomorphology 138, 443–462 (2019). https://doi.org/10.1007/s00435-019-00462-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-019-00462-4