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Silks and Silk-Producing Organs of Neotropical Tarantula Avicularia Metallica (Araneae, Mygalomorphae, Theraphosidae)

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Silks and Silk-Producing Organs of Neotropical Tarantula Avicularia Metallica (Araneae, Mygalomorphae, Theraphosidae) Research Article ISSN 2336-9744 (online) | ISSN 2337-0173 (print) The journal is available on line at www.biotaxa.org/em Silks and silk-producing organs of Neotropical tarantula Avicularia metallica (Araneae, Mygalomorphae, Theraphosidae) JAROMÍR HAJER, SIMONA KARSCHOVÁ & DANA ŘEHÁKOVÁ Department of Biology, J.E. Purkinje University, České mládeže 8, 400 96 Ústí nad Labem, Czech Republic Corresponding author: Jaromír Hajer, Department of Biology, J.E. Purkinje University, České mládeže 8, Ústí nad Labem 40096, Czech Republic. E-mail: [email protected], http://sci.ujep.cz Received 10 July 2016 │ Accepted 1 September 2016 │ Published online 2 September 2016. Abstract Silks and silk-producing organs of the theraphosid species Avicularia metallica were studied using scanning electron microscopy. The spinning apparatus is made up of two pairs of spinnerets located at the end of the ventral side of the opisthosoma. Both pairs of spinnerets are equipped with spigots (modified setae), i.e. external outlets of silk-producing glands which, in the case of posterior lateral spinnerets, are present on all three segments. The secreted silk, which hardens when exposed to air, is processed by movements of spinnerets and the opisthosoma. An investigation of spinning activity revealed two different manners in which silk is affixed to the ground: (1) by smearing silk secretion directly onto the surface of the substratum; or (2) by attaching silken fibers onto a layer of adhesive silk of attachment fields. The fibers connecting the walls of tubular shelters to the silk of attachment fields are essentially bundles of parallel nanofibrils. The connection between multifibrillar connecting fibers and the adhesive silk of attachment fields is, in essence, “silk-to-silk” connection. Nanoglobules (spherical subunits) are the basic microstructural blocks in the studied silk materials irrespective of whether the fibrils are a part of the tube, connecting fibers, or attachment fields. SEM images showed that the liquid silk, running through spigot ducts, has two components, which do not mix as they leave the spigots. The peripheral component of the solidified protein mixture surrounds the central component, which has a granular appearance. Key words: spiders, spinnerets; spigots; silk microstructure. Introduction Evolution of the order Araneae most likely occurred along three major evolutionary lines, currently represented by the infraorders Mesothelae, Mygalomorphae, and Araneomorphae (Coddington & Levi 1991). The infraorders exhibit differences in the structure of some important organs, the most remarkable of which is the silk-producing organ. The silk-spinning apparatus of spiders consists of spinnerets and silk spinning glands located in the opisthosoma. These glands originate from ectodermal invaginations on the embryonic spinneret limb buds, in relation to the morphogenesis of these buds (Hilbrant & Damen 2015). The saclike silk glands of a spider are lined by a secretory epithelium that is supported by a basal lamina and that secretes silk secretion into the glandular lumen (Kovoor 1987). Silk spinning glands supply sets of spigots (nozzles), which are generally regarded as modified setae (Bond 1994). The epithelial cells are capable of producing different types of silk secretions which consist of liquid fibroin proteins. Spider silks are viscoelestic polymers that change their material properties as they are stretched (Blackledge 2012). The silk fibers that are spun from these secretions are used in different and unique ways such as draglines, snares, Ecol. Mont., 7, 2016, 313-327 SILKS IN AVICULARIA METALLICA egg sacs and shelters (Foelix 2011). Although the molecular structure of silk fibers is fairly well understood, the hierarchical organization and complexity of constituents in the silk fibers remain poorly understood (Cranford 2013; Sampath & Yarger 2015). Spinnerets are highly modified opisthosomal appendages. Kautzch (1910) found that in the spider Agelena labyrinthica (Clerck, 1757) respiratory organs have developed extremities on the bases of the 8th and 9th body segments, and external spinning organs on the 10th and 11th segments. Yoshikura (1955) confirmed Kautzch‟s conclusion in his study of the spider Heptathela kimurai Kishida, 1920 (Mesothelae). In the paper above, Yoshikura also found that the two lateral pairs of spinnerets appear first, followed by the bases of the 10th and 11th segments of extremities; he further found that the two median pairs become separated only in the postembryonic stage. The oldest known silk-producing spigots date back to the Middle Devonian of Gilboa, New York, USA (Shear et al. 1989). The spinneret found was very much like the posterior median spinnerets of the spider infraorder Mesothelae (Selden et al. 2008). The Mesothelae are the most archetypal of recent spiders known (Haupt 2003). The most thoroughly described genera are Liphistius Schiödte, 1849, from South and South-East Asia, and Heptathela Kishida, 1923, which includes 33 species from Japan, Vietnam and China (World Spider Catalog 2016). Liphistius has four pairs of spinnerets: two pairs of multisegmental lateral and two pairs of monosegmental median. In Heptathela kimurai the posterior and the median pairs of spinnerets merge to form a single unpaired spinneret without spinning capabilities (Haupt & Kovoor 1993; Haupt 2003). Except for the Mesothelae, four pairs of spinnerets are never present, since an anterior median pair has not developed. The Araneomorphae, known as „true spiders‟, with the largest number of species, possess three pairs of spinnerets, namely the anterior lateral (ALS), posterior median (PMS), and posterior lateral spinnerets (PLS). In some spiders of the infraorder Araneomorphae, the spinning apparatus includes a functional homolog of anterior median spinnerets called the cribellum. In other true spiders, the alternative homolog of anterior lateral spinnerets is nonfunctional colulus (Kovoor 1987). Most reviews, books and journal articles on spider silk production, its molecular composition or physical/mechanical processing, have focused on understanding the dragline silk of araneomorphs. Dragline silk is an extracellular fibrous protein called spidroin, which exhibits a unique combination of strength and toughness (Tian et al. 2013). Taut dragline fibers are connected to the substratum by means of attachment discs. Anchored to the substratum by attachment discs, the “silk track” allows the spider to return safely to the starting point after a thrust at prey or following a free fall; it also allows spiderlings to maintain contact with the parental web. The same silk is used as a bridge lines and ballooning threads (Blackledge 2012). Dragline silk is produced by the secretory activity of a pair of major ampullate glands (Glandulae ampullaceae major), while the material of attachment discs is secreted by piriform glands (Glandulae piriformes) (Kovoor, 1987). The spigots of both types of glands are located on the surface of anterior lateral spinnerets. In the majority of recent spiders of the infraorders Mygalomorphae and Araneomorphae, the spinnerets are located at the posterior end of the abdomen. One of the prominent features of spiders of the infraorder Mygalomorphae, which, like Mesothelae, often live in tubular silken shelters, is the tendency to a reduction in the number of spinnerets, which undoubtedly results in a limited diversity of spinning glands, spigots, and produced silk. In all mygalomorphs the anterior median spinnerets are completely extinct, and a great number of these spiders also have reduced or nonfunctional anterior lateral spinnerets. Few scientific studies on the silk and silk-producing organs of mygalomorph spiders have been published to date. Glatz (1972, 1973) has studied the spinning apparatuses of Atypus affinis Eichwald, 1830, Atypus piceus (Sulzer, 1776) (Atypidae), Nemesia caementaria Latreille, 1799 (Nemesiidae) and Hexathele hochstetteri Ausserer, 1871 (Hexathelidae). Glatz‟s papers above include information on morphology of spinnerets and spigots and also on histology of the spinning glands. Palmer et al., (1982) has described the spinnerets and silk glands of the mygalomorph species Antrodiaetus unicolor (Hentz, 1842) (Antrodiaetidae). Palmer (1985) has also described the silk and silk production of the funnel-web spider of the genus Euagrus Thorell, 1881 (Dipluridae). Hajer (1994) examined spinning apparatus of juveniles of three Atypus species. In total 46,058 spider species belonging to 3,988 genera and 114 families are known (World Spider Catalog, 2016). Of this number, 2,720 species belong to the infraorder Mygalomorphae. The ultrastructure of silk produced by the family Theraphosidae (common name: tarantulas, or baboon spiders), which includes the largest recent spiders and which is the most numerous family of the infraorder Mygalomorphae with its 314 HAJER ET AL. 132 genera and 953 species (World Spider Catalog, 2016), has not yet been investigated. The spinning apparatus of Theraphosidae consists of two pairs of spinnerets in which aciniform spinning glands supply one type of spigots (Murphy & Roberts 2015: 57, 220–221). The family is divided into ten subfamilies, and the genus Avicularia Lamarck, 1818, belongs to the subfamily Aviculariinae, which is endemic to South America. Like most spiders of the genus Avicularia, the species under investigation, Avicularia metallica, Ausserer, 1875, is one of the arboreal and rain forest species found in silken tube retreats in
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