Research Article |
Corresponding author: Gero Hilken ( gero.hilken@uk-essen.de ) Academic editor: Ivan H. Tuf
© 2015 Gero Hilken, Gregory D. Edgecombe, Carsten H.G. Mueller, Andy Sombke, Christian S. Wirkner, Jörg Rosenberg.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Hilken G, Edgecombe GD, Müller CHG, Sombke A, Wirkner CS, Rosenberg J (2015) Interaction of the tracheal tubules of Scutigera coleoptrata (Chilopoda, Notostigmophora) with glandular structures of the pericardial septum. In: Tuf IH, Tajovský K (Eds) Proceedings of the 16th International Congress of Myriapodology, Olomouc, Czech Republic. ZooKeys 510: 233-242. https://doi.org/10.3897/zookeys.510.8644
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Notostigmophora (Scutigeromorpha) exhibit a special tracheal system compared to other Chilopoda. The unpaired spiracles are localized medially on the long tergites and open into a wide atrium from which hundreds of tracheal tubules originate and extend into the pericardial sinus. Previous investigators reported that the tracheal tubules float freely in the hemolymph. However, here we show for the first time that the tracheal tubules are anchored to a part of the pericardial septum. Another novel finding is this part of the pericardial septum is structured as an aggregated gland on the basis of its specialized epithelium being formed by hundreds of oligocellular glands. It remains unclear whether the pericardial septum has a differently structure in areas that lack a connection with tracheal tubules. The tracheal tubules come into direct contact with the canal cells of the glands that presumably secrete mucous substances covering the entire luminal cuticle of the tracheal tubules. Connections between tracheae and glands have not been observed in any other arthropods.
Centipedes, electron microscopy, tracheal system, aggregated recto-canal epidermal glands, respiration
The history of research on tracheae of Scutigera coleoptrata extends back to the 19th century.
During recent years, we focused on tracheal systems (
Specimens of Scutigera coleoptrata (Linnaeus, 1758) were reared in glass boxes filled with 1 cm soil substrate and moistened tissues and fed with Drosophila sp. and Musca sp. Animals were anesthetized with CO2, subsequently fixed, cut along the tergite edges, and preserved as described below.
For scanning electron microscopic (SEM) investigations of the tracheal tubules, whole specimens were fixed in ethanol (70%). Tracheae were macerated using pepsin. Optimal results were obtained with a solution of 1–2 g pepsin in 100 ml HCl (37%,
For light microscopic (LM) and transmission electron microscopic (TEM) investigations, segments of Scutigera coleoptrata were fixed in phosphate buffered paraformaldehyde (4%, pH 7.2), containing 15% saturated picric acid and 0.08% glutaraldehyde. They were postfixed with 1% OsO4 in the same buffer and, after alcohol dehydration, embedded in Epon. Semithin sections (0.5–1 µm) were stained with 1% toluidine blue in a solution of 1% sodium tetraborate. Sections were studied using a DMSL-Leica microscope. Ultrathin sections were stained with uranyl acetate and lead citrate and studied using a ZEISS EM 902 A electron microscope.
The unpaired openings or spiracles of the tracheal system of Scutigera coleoptrata are located dorsomedially on each of the seven long tergites (Fig.
Tracheal system and pericardial septum of Scutigera coleoptrata. A Spiracle (stomata) situated dorsomedially on long tergite 4 (SEM) B Tracheal system with its atrium and hundreds of tracheal tubules (SEM) C Cross-section of tracheal system with its tracheal tubules within the pericardial sinus. The sinus is surrounded by the specialized part of the pericardial septum (LM) D Inset showing details of the tergal cuticle with epidermis and the pericardial septum. The tracheal tubules extend into the epithelium of the pericardial septum (LM) E Overview of the epithelium of the pericardial septum with endings of two tracheal tubules and nuclei of glandular units (TEM) F Detail of a glandular unit within the pericardial septum consisting of a secretory cell, an intermediary cell, and a canal cell. In the secretory cell, parts of the microvilli of the secretory reservoir are visible, as are parts of the canaliculi system in the intermediary cell. a atrium, bc body cavity; bl basal lamina, c, cuticle, ca canaliculi system, cc canal cell, ic intermediary cell, e epidermis, gu glandular unit, h dorsal heart, mu body muscle; n nuclei of glandular unit cells, pc pericardial cavity; ps pericardial septum, s spiracle, sc secretory cell, sr reservoir of the secretory cell, te tergite, tt tracheal tubules
Pericardial glands and mucoid substances. A Longitudinal section of a connection of the tip of a tracheal tubule and a canal cell of a glandular unit B Cross section of a connection between a tracheal tubule and a canal cell of a glandular unit C Tracheal tubule in the vicinity of a glandular unit. The tracheal tubule is filled with mucoid substances D Cross section of the ending of a tracheal tubule surrounded by the epithelium of a glandular unit. The tracheal lumen is filled with different mucoid substances E Longitudinal section of a tracheal tubule near the pericardial septum filled with electron-dense and electron-lucent mucoid substances F Part of a longitudinal section of a tracheal tubule. The specialized cuticle is covered by mucoid substances G Oblique section of a tracheal tubule. The tracheal cuticle is covered by a distinct mucoid substance. bl basal lamina; c cuticle; cc canal cell; cd cuticular duct of the canal cell; ed electron-dense fraction of mucous; el electron-lucent fraction of mucus; ic intermediary cell; m mucoid substance; sc secretory cell, sr secretory reservoir; te tracheal epithelium; tt tracheal tubules; arrows, presumed interdigitations between tracheae and glandular compartment.
In Scutigera coleoptrata the length of the tracheal tubules ranges from 150–200 µm (Fig.
The pericardial septum arises from the atrium, partly accompanies the tergal epidermis, and delimits the hemolymph sinus against the body muscles (Fig.
The polarity of the pericardial septum is characterized by the development of a distinct basal lamina against the body cavity (Fig.
We are now able to resolve previous confusion on the length and connectivity of tracheal tubules of scutigeromorph centipedes. Whereas the majority of reports thus far considered tracheal tubules to end freely in the tracheal sinus compartments (e.g.
The structure and position of scutigermorph (notostigmophoran) tracheal systems are unique among Chilopoda (
Recently, there has been a particular increase in knowledge of epidermal glands of various degrees of organization in Chilopoda. It is possible to distinguish four classes of epidermal glands: 2-cell-glands (composed of a single secretory cell and a single canal cell), 3-cell-glands (composed of a proximal secretory cell, an intermediary cell, and a distal canal cell), 4-cell-glands (composed of a proximal secretory cell, an intermediary cell, a distal canal cell, and a proximal canal cell), and 5-cell glands (composed of two secretory cells, an intermediary cell, a distal canal cell, and a proximal canal cell) (see Table 2 in
Many features indicate that the glands in question strongly resemble aggregated recto-canal glands in the epidermis. These include the following: (1) the structure of the glands associated with the tracheae; (2) the universal tricellular construction of the glandular units (consisting of a canal cell, an intermediary cell, and a secretory cell); (3) the presence of an intermediary cell surrounding an almost non-cuticularized duct; and (4) the independent release of a secretion of every glandular unit into the tracheal tubules via its own duct. Thus, an epidermal origin of the tracheae-associated glands cannot be excluded. In no other arthropods are connections between tracheae and multicellular glands observed. Future studies are needed to unravel the cellular diversity, functional complexity, distribution, and organization of the pericardial septum as a whole.
The closely adjoined glandular units release their secretion via canal cells into the connected tracheal tubules. It is likely that each secretory gland secretes mucous substances into the tracheal tubules which cover the luminal side of the cuticle of each tracheal tubule along its entire extension.