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Introvert, mouth cone, and nervous system of Echinoderes capitatus (Kinorhyncha, Cyclorhagida) and implications for the phylogenetic relationships of Kinorhyncha

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Summary

The introvert, mouth cone, and nervous system of Echinoderes capitatus were examined by transmission and scanning electron microscopy. The introvert bears seven rings of primarily quincunxial sensory scalids, including type 1 and 2 spinoscalids as well as trichoscalids; the latter two types are additionally provided with glandular cells. The mouth cone bears one ring of decamerous sensory oral styles and three rings of quincunxial sensory pharyngeal styles. The intra- to basiepithelial, bilateral nervous system consists of a circumentric nerve ring in the introvert, a terminal and proximal nerve ring in the mouth cone, a ventral chain of ganglia, one in each trunk zonite, and a caudal ganglion. The introvert, the neck, and the trunk zonites are innervated from the forebrain; the mouth cone and the pharyngeal bulb are innervated from the hindbrain. The monophyly of the Kinorhyncha is based upon the following autapomorphic characters: (1) a mouth cone, (2) a neck with 16 placids, (3) a trunk with 11 zonites, (4) scalids of three types: type 1 and type 2 spinoscalids, and trichoscalids, (5) an anteriormost ring of ten type 1 spinoscalids (sensory organs divided into a basal and a terminal part), (6) a posteriormost ring of 14 trichoscalids (glandular sensory organs which are undivided), (7) rings in between the anteriormost and posteriormost are type 2 spinoscalids (glandular sensory organs divided into a basal and a terminal part), (8) a mouth cone with a terminal and a proximal nerve ring, (9) nine sensory oral styles with decamerous symmetry (the dorsal style is missing) and (10) three rings of sensory pharyngeal styles with, from anterior to posterior, ten, five, and five styles with quincunxial arrangement. The following characters are assumed to be autapomorphic for the taxon Nematoda+Gastrotricha+Kinorhyncha+Loricifera+Priapulida: (1) a basiepithelial circumentric brain and (2) a neuropileous nerve ring in a subterminal position. The following characters are assumed to be autapomorphic for the taxon Kinorhyncha+Loricifera+Priapulida: (1) a neuropileous nerve ring in a terminal position, (2) an introvert with scalids, (3) an eversible foregut and (4) tanycytes.

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References

  • Adrianov AV, Malakhov VV (1990) Sense organs of Kinorhyncha using the example of the order Homalorhagida (Cephalorhyncha, Kinorhyncha) (in Russian). Zool Zh 9:1–14

    Google Scholar 

  • Apel W (1885) Beitrag zur Anatomie und Histologie des Priapulus caudatus (Lam.) und des Halicryptus spinulosus (v. Sieb.). Z Wiss Zool 42:459–529

    Google Scholar 

  • Ax P (1984) Das phylogenetische System. Systematisierung der lebenden Natur aufgrund ihrer Phylogenese. Fischer, Stuttgart New York, pp 349

    Google Scholar 

  • Brown R (1989) Morphology and ultrastructure of the sensory appendages of a kinorhynch introvert. Zool Scr 18:471–482

    Google Scholar 

  • Bullock TH, Horridge GA (1965) Structure and function of the nervous system of invertebrates (2 vols). Freeman, San Francisco, vol 1: 789 pp, vol 2: 1719 pp

    Google Scholar 

  • Calloway CB (1975) Morphology of the introvert and associated structures of the priapulid Tubiluchus corallicola from Bermuda. Mar Biol 31:161–174

    Google Scholar 

  • Candia Carnevali MD, Ferraguti M (1979) Structure and ultra-structure of muscles in the priapulid Halicryptus spinulosus: functional and phylogenetic remarks. J Mar Biol Assoc UK 59:737–744

    Google Scholar 

  • Chitwood BG, Chitwood MB (1974) Introduction to nematology. University Park Press, Baltimore, pp 334

    Google Scholar 

  • Clark RB (1964) Dynamics in metazoan evolution. Claredon Press, Oxford, pp 313

    Google Scholar 

  • Clark RB (1979) Radiation of the metazoa. In: House MR (ed) The origins of major invertebrate groups, Systematic association special volume 12. Academic Press, London New York, pp 55–102

    Google Scholar 

  • Clèment P (1985) The relationships of rotifers. In: Conway Morris S, George JD, Gibson R, Platt HM (eds) The origin and relationships of lower invertebrates. The systematic association special volume 28. Claredon Press, Oxford, pp 224–247

    Google Scholar 

  • Clèment P, Wurdak E (1991) Rotifera. In: Harrison FW (ed) Microscopic anatomy of invertebrates vol 4: Aschelminthes. Wiley and Sons, New York, pp 219–297

    Google Scholar 

  • Conway Morris S (1977) Fossil priapulid worms. Spec Pap Palacont 20:1–95

    Google Scholar 

  • Crompton DWT, Nickol BB (1985) Biology of the Acanthocephala. Cambridge University Press, Cambridge London New York, pp 519

    Google Scholar 

  • Elder HY, Hunter RD (1980) Burrowing of Priapulus caudatus (Vermes) and the significance of the direct peristalitic wave. J Zool Lond 191:333–351

    Google Scholar 

  • Eldredge N, Cracraft J (1980) Phylogenetic patterns and the evolutionary process. Methods and theory in comparative biology. Columbia University Press, New York, pp 349

    Google Scholar 

  • Friedrich H, Langeloh H-P (1936) Untersuchungen zur Physiologie der Bewegung und des Hautmuskelschlauches bei Halicryptus spinulosus and Priapulus caudatus. Biol Zbl 56:249–260

    Google Scholar 

  • Gerlach SA (1956) Über einen aberranten Vertreter der Kinorhynchen aus dem Küstengrundwasser. Kieler Meeresforsch 12:120–124

    Google Scholar 

  • Goldschmidt R (1908) Das Nervensystem von Ascaris lumbricoides und megalocephela I. Z Wiss Zool 90:73–136

    Google Scholar 

  • Goldschmidt R (1909) Das Nervensystem von Ascaris lumbricoides und megalocephela II. Z Wiss Zool 92:306–357

    Google Scholar 

  • Hammersten O (1913) Beiträge zur Entwicklung von Halicryptus spinulosus (von Siebold). Zool Anz 41:501–505

    Google Scholar 

  • Hammersten O (1915) Zur Entwicklungsgeschichte von Halicryptus spinulosus (von Siebold). Z Wiss Zool 112:527–571

    Google Scholar 

  • Hammond RA (1970) The surface of Priapulus caudatus (Lamarck, 1816) Nemathelminthes, Priapulida. Z Morphol Tiere 68:255–268

    Google Scholar 

  • Higgins RP (1967) The Kinorhyncha of New Caledonia. In: Expedition francaise sur récifs coralliens de la Nouvelle-Caledonia 2, edition de la fondation Singer-Polignac, Paris, pp 75–90

    Google Scholar 

  • Higgins RP (1968) Taxonomy and postembryonic development of the Cryptorhagae, a new suborder for the mesopsammic kinorhynch genus Cateria. Trans Am Microsc Soc 78:21–39

    Google Scholar 

  • Higgins RP (1969a) Indian Ocean Kinorhyncha, 1: Condyloderes and Sphenoderes, new cyclorhagid genera. Smithson Contrib Zool 14:1–13

    Google Scholar 

  • Higgins RP (1969b) Indian Ocean Kinorhyncha, 2: Neocentrophyidae, a new homalorhagid family. Proc Biol Soc Wash 82:113–128

    Google Scholar 

  • Higgins RP (1981) Kinorhyncha. In: Parker SP (ed) Synopsis and classification of living organisms, vol 1. McGraw-Hill, New York, pp 873–877

    Google Scholar 

  • Higgins RP (1983) The Atlantic Barriere reef ecosystem at Carrie Bow Cay, Belize. II: Kinorhyncha. Smithson Contrib Mar Sci 18:1–131

    Google Scholar 

  • Higgins RP (1990) Zelinkaderidae, a new family of cyclorhagid Kinorhyncha. Smithson Contrib Zool 500:1–26

    Google Scholar 

  • Higgins RP, Kristensen RM (1986) New Loricifera from Southeastern United States coastal waters. Smithson Contrib Zool 438:1–70

    Google Scholar 

  • Higgins RP, Shirayama Y (1990) Dracoderidae, a new family of cyclorhagid Kinorhyncha from the inland sea of Japan. Zool Sci 7:939–946

    Google Scholar 

  • Higgins RP, Storch V (1989) Ultrastructural observations of the larva of Tubiluchus corallicola (Priapulida). Helgo Meeresunters 43:1–11

    Google Scholar 

  • Higgins RP, Storch V (1991) Evidence for direct development in Meiopriapulus fijiensis (Priapulida). Trans Am Microsc Soc 110/1: 37–46

    Google Scholar 

  • Hyman LH (1951) The Invertebrates: Acanthocephala, Aschelminthes, and Ectoprocta. The pseudocoelomate Bilateria. McGraw-Hill, New York Toronto London, pp 572

    Google Scholar 

  • Johnston TH (1938) Report on the Echinoderida. Reports on the Australian Antarctic expedition, 1911–1914 (C). Paisley, Sydney New South Wales Australia, 10/7:1–13

    Google Scholar 

  • Kirsteuer E (1976) Notes on adult morphology and larval development of Tubiluchus corallicola (Priapulida), based on in vivo and scanning electron, microscopic examinations of specimens from Bermuda. Zool Scr 5:239–255

    Google Scholar 

  • Kirsteuer E, Rüitzler K (1973) Additional notes on Tubiluchus corallicola (Priapulida), based on scanning electron microscope observations. Mar Biol 20:78–87

    Google Scholar 

  • Kirsteuer E, van der Land J (1970) Some notes on Tubiluchus corallicola (Priapulida) from Barbados, West Indies. Mar Biol 7:230–238

    Google Scholar 

  • Kristensen RM (1983) Loricifera, a new phylum with Aschelminthes characters from the meiobenthos. Z Zool Syst Evolutionsforsch 21:163–180

    Google Scholar 

  • Kristensen RM (1991a) Loricifera. In: Harrison FW (ed) Microscopic anatomy of invertebrates, vol 4: Aschelminthes. Wiley and Sons, New York, pp 351–375

    Google Scholar 

  • Kristensen RM (1991b) Loricifera — a general biological and phylogenetic overview. Verh Dtsch Zool Ges 84:231–246

    Google Scholar 

  • Kristensen RM, Hay-Schmidt A (1989) Protonephridia of the Arctic Kinorhynch Echinoderes aquilonius (Cyclorhagida, Echinoderidae). Acta Zool (Stockholm) 70:13–27

    Google Scholar 

  • Kristensen RM, Higgins RP (1991) Kinorhyncha. In: Harrison FW (ed) Microscopic anatomy of invertebrates, vol 4: Aschelminthes. Wiley and Sons, New York, pp 377–404

    Google Scholar 

  • Kristensen RM, Shirayama Y (1988) Pliciloricus hadalis (Pliciloricidae), a new loriciferan species collected from the Izu-Ogasawara Trench, Western Pacific. Zool Sci 5:875–881

    Google Scholar 

  • Land J van der (1968) A new aschelminth, probably related to the Priapulida. Zool Meded 42:237–250

    Google Scholar 

  • Land J van der (1970) Systematics, zoogeography, and ecology of the Priapulida. Zool Verhandl Leiden 12:1–118

    Google Scholar 

  • Land J van der, Nørrevang A (1985) Affinities and intraphyletic relationships of the Priapulida. In: Conway Morris S, George JD, Gibson R, Platt HM (eds) The origin and relationships of lower invertebrates. The systematic association special vol. 28. Claredon Press, Oxford, pp 261–273

    Google Scholar 

  • Lang K (1949) Reports of the Lund University Chile Expedition 1948–49: Echinoderida. K Fysiogr Sällsk Lund Förh 64:1–8

    Google Scholar 

  • Lang K (1963) The relation between Kinorhyncha and Priapulida and their connection with the Aschelminthes. In: Dougherty EC (ed). The lower Metazoa, comparative biology and phylogeny. University of California Press, Berkeley pp 256–262

    Google Scholar 

  • Lorenzen S (1985) Phylogenetic aspects of pseudocoelomate evolution. In: Conway Morris S, George JD, Gibson R, Platt HM (eds) The origin and relationships of lower invertebrates. The systematic association special vol 28. Claredon Press, Oxford, pp 210–223

    Google Scholar 

  • Malakhov VV (1980) Cephalorhyncha, a new type of animal kingdom uniting Priapulida, Kinorhyncha, Gordiacea, and a system of aschelminthes worms (in Russian). Zool Zh 59:485–499

    Google Scholar 

  • Mattisson A, Nilsson S, Fänge R (1974) Light microscopical and ultrastructural organization of muscles of Priapulus caudatus (Priapulida) and their responses to drugs, with phylogenetic remarks. Zool Scr 3:209–218

    Google Scholar 

  • Merriman JA, Corwin HO (1973) An electron microscopical examination of Echinoders dujardini Claparède (Kinorhyncha). Z Morphol Tiere 76:227–242

    Google Scholar 

  • Moore PG (1973) Campyloderes macquariae Johnston, 1938 (Kinorhyncha: Cyclorhagida) from the northern hemispere. J Nat Hist 7:341–353

    Google Scholar 

  • Moritz K, Storch V (1972a) Zur Feinstruktur des Integumentes von Trachydemus giganteus (Kinorhyncha). Z Morphol Tiere 71:189–202

    Google Scholar 

  • Moritz K, Storch V (1972b) Über den ultrastrukturellen Bau der Skaliden von Trachydemus giganteus (Kinorhyncha). Mar Biol 16:81–89

    Google Scholar 

  • Morse MP (1981) Meiopriapulus fijiensis n. gen., n. sp.: an interstitial priapulid from coarse sand in Fiji. Trans Am Microsc Soc 100:239–252

    Google Scholar 

  • Nebelsick M (1990) Antygomonas incomitata gen. et sp.n. (Cyclorhagida, Kinorhyncha) and its phylogenetic relationships. Zool Scr 19/2:143–152

    Google Scholar 

  • Nebelsick M (1992a) Sensory spots of Echinoderes capitatus (Kinorhyncha, Cyclorhagida). Acta Zool (Stockholm) 73/3:185–195

    Google Scholar 

  • Nebelsick M (1992b) Ultrastructural investigations of three taxonomic characters in the trunk region of Echinoderes capitatus (Kinorhyncha, Cyclorhagida). Zool Scr 21/4:335–345

    Google Scholar 

  • Por FD, Bromley HJ (1974) Morphology and anatomy of Maccabeus tentaculatus (Priapulida: Seticoronaria). J Zool Lond 173:173–197

    Google Scholar 

  • Purasjoki KJ (1944) Beiträge zur Kenntnis der Entwicklung und Ökologie der Halicrypus spinulosus-Larve (Priapulida). Ann Soc Zool Bot Fenn 9/6:1–14

    Google Scholar 

  • Rauter M (1930) Fünfte Klasse des Cladus Nemathelminthes Nematomorpha=Saitenwürmer. In: Kükenthal W, Krumbach T (eds) Handbuch der zoologie 2. Walter de Gruyter, Berlin, pp 404–448

    Google Scholar 

  • Rehkämper G, Storch V, Alberti G, Welsch U, (1989) On the fine structure of the nervous system of Tubiluchus philippinensis (Tubiluchidae, Priapulida). Acta Zool (Stockholm) 70/2:111–120

    Google Scholar 

  • Remane A (1929) Dritte Klasse des Cladus Nemathelminthes Kinorhyncha=Echinodera. In: Kükenthal W, Krumbach T (eds) Handbuch der zoologie 2. Walter de Gruyter, Berlin, pp 187–248

    Google Scholar 

  • Remane A (1936) Gastrotricha und Kinorhyncha. In: Bronn HG (ed) Klassen und Ordnungen des Tierreichs (sec 2, pt 1, no 2) 4. Akad Verlagsges, Leipzig, pp 243–372

    Google Scholar 

  • Rieman F (1972) Kinonchulus sattleri n.g.n.sp. (Enoplida, Tripyloidea), an aberrant freeliving nematode from the lower Amazonas. Veröff Inst Meeresforsch Bremerhaven 13:317–326

    Google Scholar 

  • Salvini-Plawen L v (1974) Zur Morphologie und Systematik der Priapulida: Chaetostephanus praeposteriens, der Vertreter einer neuen Ordnung Seticoronaria. Z Zool Syst Evolutionsforsch 12:31–54

    Google Scholar 

  • Scharff R (1885) On the skin and nervous system of Priapulus and Halicryptus. Q J Microsc Sci 25:193–213

    Google Scholar 

  • Schepotieff A (1908) Über den feineren Bau der Gordiuslarven. Z Wiss Zool 89:230–241

    Google Scholar 

  • Storch V (1984) Minor Pseudocoelomates. In: Bereiter-Hahn J, Matoltsy AG, Sylvia Richards K (eds) Biology of the integument 1. Invertebrates. Springer, Berlin Heidelberg New York, pp 242–268

    Google Scholar 

  • Storch V, Higgins RP (1991) Scanning and transmission electron microscopic observations on the larvae of Halicryptus spinulosus (Priapulida). J Morphol 210:175–194

    Google Scholar 

  • Storch V, Higgins RP, Morse MP (1989) Internal anatomy of Meiopriapulus fijiensis (Priapulida). Trans Am Microsc Soc 108/3:245–261

    Google Scholar 

  • Storch V, Higgins RP, Rumohr H (1990) Ultrastructure of introvert and pharynx of Halicryptus spinulosus (Priapulida). J Morphol 206:163–171

    Google Scholar 

  • Teuchert G (1977) The ultrastructure of the marine gastrotrich Turbanella cornuta Remane (Macrodasyoidea) and its functional and phylogenetic importance. Zoomorphologie 88:189–246

    Google Scholar 

  • Trueman ER (1968) Burrowing habit and the early evolution of body cavities. Nature (Lond) 218:96–98

    Google Scholar 

  • Ware RW, Clark C, Crossland K, Russell RL (1975) The nerve ring of the nematode, Caenorhabditis elegans. J Comp Neurol 162:71–110

    Google Scholar 

  • Welsch U, storch V (1973) Einführung in die Cytologie und Histologie der Tiere. Fischer, Stuttgart, 244 pp

    Google Scholar 

  • White JG, Southgate E, Thomson JN, Brenner FRS (1976) The structure of the ventral nerve chord of Caenorhabditis elegans. Phil Trans R Soc Lond B 275:327–348

    Google Scholar 

  • White JG, Southgate JN, Thomson JN, Brenner FRS (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Phil Trans R Soc Lond B 314:1–340

    Google Scholar 

  • Whitefield PJ (1984) Acanthocephala In: Bereiter-Hahn J, Matoltsy AG, Sylvia Richards K (eds) Biology of the integument 1. Invertebrates. Springer, Berlin Heidelberg New York, pp 234–241

    Google Scholar 

  • Zelinka K (1928) Monography of Echinodera. Engelmann, Leipzig, 360 pp

    Google Scholar 

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  1. Abteilung für Meeresbiologie und Ultrastrukturforschung, Institut für Zoologie, Universität Wien, Althanstrasse 14, A-1090, Wien

    Monika Nebelsick

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The unpublished doctoral thesis of B. Neuhaus [1991 Zur Ultrastruktur, Postembryonalentwicklung und phylogenetischen Verwandtschaft der Kinorhyncha. PhD thesis. University of Götingen, Germany] was finished simultaneously with the completion of this study.

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Nebelsick, M. Introvert, mouth cone, and nervous system of Echinoderes capitatus (Kinorhyncha, Cyclorhagida) and implications for the phylogenetic relationships of Kinorhyncha. Zoomorphology 113, 211–232 (1993). https://doi.org/10.1007/BF00403313

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