Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-20T04:47:05.709Z Has data issue: false hasContentIssue false
  • English
  • Français

A preliminary account of the general and enzyme histochemistry of Siboglinum atlanticum and other Pogonophora

Published online by Cambridge University Press:  11 May 2009

C. Eve  and
A. J. Southward
C. Eve
Affiliation:
The Plymouth Laboratory
A. J. Southward
Affiliation:
The Plymouth Laboratory
Get access Rights & Permissions [Opens in a new window]

Extract

An account is given of the distribution of certain polysaccharides, lipids and proteins in the tissues of Siboglinum atlanticum, a uni-tentaculate pogonophore collected from depths of 1300–1500 m on the continental slope. The histology of the various glands and cells is described, and the structure and histochemistry of the tentacle compared with that of three multitentaculate species of pogonophores collected from similar habitats.

Esterases hydrolysing a naphthyl acetate and o-acetyl-bromoindoxyl are found in most tissues of Siboglinum after formalin fixation. An eserine-sensitive esterase was present in the dorsal ciliated band, mostly close to the bases of the cilia. An organophosphorus-resistant esterase was widely distributed as scattered particles in the subcuticular region of the epidermis of the tentacle and anterior end. The other tissues, including the epidermal glands, blood vessels, muscles and peritoneum, contained a simple B-esterase which was closely associated with lipid globules; the nerve fibre B-esterase was not associated with lipid and its apparent sensitivity to copper illustrates one aspect of the difficulty of applying mammalian esterase subdivisions to invertebrates. Lipids form the main food reserve, and appear to have a dominant role in the metabolism.

Pogonophores do not possess a gut at any stage in their life, and must take up food through the epidermis, whether or not it is first digested. The epidermal glands do not appear to have any digestive function. The multicellular pyriform glands secrete fibres of chitin and acid mucopolysaccharide, and produce the major part of the tube in which the animal lives. The unicellular glands are of several types, but most of them, apart from some simple mucous glands, appear to take part in tube formation, secreting mucopolysaccharides or mucopolysaccharides and protein.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 46 , Issue 3 , October 1966 , pp. 579 - 616
Copyright
Copyright © Marine Biological Association of the United Kingdom 1966

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, C. W. M. & Tuqan, N. A. 1960. The histochemical demonstration of protease by a gelatin-silver film substrate. J. Histochem. Cytochem., Vol. 9, pp. 469–72.CrossRefGoogle Scholar
Andersen, B. & Ussing, H. H. 1960. Active transport. Comp. Biochem. Physiol., Vol. 2, pp. 371–440.CrossRefGoogle Scholar
Baird, R. H. 1955. A preliminary report on a new type of commercial escallop dredge. J. Cons. perm. int. Explor. Mer, Vol. 20, pp. 290–4.CrossRefGoogle Scholar
Baker, J. R. 1944. The structure and chemical composition of the Golgi element. Q. Jl microsc. Sci., Vol. 85, pp. 1–71.Google Scholar
Baker, J. R. 1956. The histochemical recognition of phenols, especially tyrosine. Q. Jl microsc. Sci., Vol. 97, pp. 161–74.Google Scholar
Barrington, E. J. W. 1941. Observations on feeding and digestion in Glossobalanus minutus. Q. Jl microsc. Sci., Vol. 82, pp. 227–260.Google Scholar
Barrington, E. J. W. 1962. Digestive enzymes. Adv. comp. Physiol. Biochem., Vol. 1, pp. 1–65.Google ScholarPubMed
Bergman, F.Segal, R. & Rimon, S. 1957. A new type of esterase in hog-kidney extract. Biochem. J., Vol. 67, pp. 481–6.CrossRefGoogle Scholar
Binot, D. 1965. Histologie, histochimie, cytologie de quelques formations glandulaires du tégument d'Oncidiella celtica (Cuv.) (Gastéropode pulmone). Cah. Biol. mar., T. 6, pp. 325–46.Google Scholar
Blackstad, T. W. 1963. The skin and slime glands. In The Biology of Myxine, pp. 195–230. Ed. A. Brodal and R. Fange. Oslo: Universitets-forlaget.Google Scholar
Blackwell, J.Parker, K. D. & Rudall, K. M. 1965. Chitin in pogonophore tubes. J. mar. biol. Ass. U.K., Vol. 45, pp. 659–61.CrossRefGoogle Scholar
Bresciani, J. & Fenchel, T. 1965. Studies on dicyemid Mesozoa. I. The fine structure of the adult (the nematogen and rhombogen stage). Vidensk. Meddr dansk. naturh. Foren., Bd. 128, pp. 85–92.Google Scholar
Brimacombe, J. S. & Webber, J. M. 1964. Mucopolysaccharides. Amsterdam: Elsevier.Google ScholarPubMed
Brunet, P. C. J. & Carlisle, D. B. 1958. Chitin in Pogonophora. Nature, Lond., Vol. 182, p. 1689.CrossRefGoogle Scholar
Bülbring, E.Burn, J. H. & Shelley, H. J. 1953. Acetylcholine and ciliary movement in the gill plates of Mytilus edulis. Proc. R. Soc. B, Vol. 141, pp. 445–66.Google Scholar
Bullock, W. L. 1949. Histochemical studies on the Acanthocephala I. The distribution of lipase and phosphatase. J. Morph., Vol. 84, pp. 185–99.CrossRefGoogle ScholarPubMed
Burstone, M. S. 1962. Enzyme Histochemistry and its Application to the Study of Neoplasms. New York: Academic Press.Google Scholar
Campion, M. 1961. The structure and function of the cutaneous glands in Helix aspersa. Q. Jl microsc. Sci., Vol. 102, pp. 191–216.Google Scholar
Caullery, M. 1944. Siboglinum Caullery 1914 type nouveau d'invertébrés, d'affinités à préciser. Siboga Exped., Monogr. 25 bis, 26 pp.Google Scholar
Dales, R. P. 1955. Feeding and digestion in terebellid polychaetes. J. mar. biol. Ass. U.K., Vol. 34, pp. 55–79.CrossRefGoogle Scholar
Dales, R. P. 1961. The coelomic and peritoneal cell systems of some sabellid polychaetes. Q. Jl microsc. Sci., Vol. 102, pp. 327–46.Google Scholar
Dixon, M. & Dixon, B. R. 1966. Uptake of small particles by Moniliformis dubius (Acanthocephala). Nature, Lond., Vol. 209, p. 99.Google Scholar
Fawcett, D. W. 1965. Surface specialisations of absorbing cells. J. Histochem. Cytochem., Vol. 13, pp. 75–91.Google Scholar
Fontaine, A. R. 1964. The integumentary mucous secretions of the ophiuroid Ophiocomina nigra. J. mar. biol. Ass. U.K., Vol. 44, pp. 145–62.Google Scholar
Forster, G. R. 1953. A new dredge for collecting burrowing animals. J. mar. biol. Ass. U.K., Vol. 32, pp. 193–8.CrossRefGoogle Scholar
Foucart, M. F.Bricteux-Gregoire, S. & Jeuniaux, C. 1965. Composition chimique du tube d'un pogonophore (Siboglinum sp.) et des formations squelettiques de deux ptérobranchs. Sarsia, No. 20, pp. 35–41.Google Scholar
Gupta, B. L.Little, C. & Philips, A. M. 1966. Studies on Pogonophora. Fine structure of the tentacles. J. mar. biol. Ass. U.K., Vol. 46, pp. 351–72.Google Scholar
Hartman, O. 1961. New Pogonophora from the eastern Pacific Ocean. Pacific Sci., Vol. 15, pp. 542–6.Google Scholar
Heath, I. D. 1962. Observations on a highly specific method for the histochemical determination of sulphated mucopolysaccharides, and its possible mechanisms. Q. Jl microsc. Sci., Vol. 103, pp. 457–75.Google Scholar
Hess, R. & Pearse, A. G. E. 1958. The histochemistry of indoxylesterase of rat kidney with special reference to its cathepsin-like activity. Br. J. exp. Path., Vol. 39, pp. 292–9.Google ScholarPubMed
Hemmingsen, E. A. 1965. Accelerated transfer of oxygen through solutions of haem pigments. Acta physiol. scand., Vol. 64, suppl. 246, 53 pp.Google Scholar
Holme, N. A. 1961. The bottom fauna of the English Channel. J. mar. biol. Ass. U.K., Vol. 41, pp. 397–461.Google Scholar
Holt, S. J. & Withers, R. F. J. 1952. Cytochemical localisation of esterases using indoxyl derivatives. Nature, Lond., Vol. 170, pp. 1012–14.Google Scholar
Ito, S. 1965. The enteric surface coat on cat intestinal microvilli. J. Cell Biol., Vol. 27, PP. 475–91.Google Scholar
Ivanov, A. V. 1955. External digestion in Pogonophora. Dokl. Akad. Nauk. SSSR, Vol. 100, pp. 381–3. (In Russian.)Google Scholar
Ivanov, A. V. 1963. Pogonophora. London: Academic Press.CrossRefGoogle Scholar
Ivanov, A. V. 1964. On the structure of the hind region of the body in Pogonophora. Zool. Zh., Vol. 43, pp. 581–9 (in Russian). Translation in Cah. Biol. mar., T. 6, pp. 311–23.Google Scholar
Jägersten, G. 1956. Investigations on Siboglinum ekmani n.sp., encountered in Skagerak, with some general remarks on the group Pogonophora. Zool. Bidr. Upps., Bd. 31, pp. 211–52.Google Scholar
Jägersten, G. 1957. On the larva of Siboglinum. Zool. Bidr. Upps., Bd. 32, pp. 67–80.Google Scholar
Jennings, J. B. 1962a. A histochemical study of digestion and digestive enzymes in the rhynchocoelan Lineus ruber (O. F. Muller). Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 122, pp. 63–72.Google Scholar
Jennings, J. B. 1962b. Further studies on feeding and digestion in triclad Turbellaria. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 123, pp. 571–81.Google Scholar
Kermack, D. 1955. The anatomy and physiology of the gut of the polychaete Arenicola marina (L.). Proc. zool. Soc. Lond., Vol. 125, pp. 347–81.Google Scholar
Lane, N. J. 1963. Microvilli on the external surfaces of gastropod tentacles and body walls. Q. Jl microsc. Set., Vol. 104, pp. 495–504.Google Scholar
Lee, D. L. 1962. The distribution of esterase enzymes in Ascaris lumbricoides. Parasitology, Vol. 52, pp. 241–60.Google Scholar
Lee, D. L. 1964. Esterase enzymes in two free-living nematodes. Proc. helminthol. Soc. Wash., Vol. 31, pp. 285–8.Google Scholar
Lee, D. L. 1965. The Physiology of Nematodes. Edinburgh: Oliver and Boyd.Google Scholar
Lee, D. L.Rothman, A. H. & Senturia, J. B. 1963. Esterases in Hymenolepis and Hydatigera. Expl Parasit., Vol. 14, pp. 285–95.CrossRefGoogle ScholarPubMed
Lee, D. L. & Tatchell, R. J. 1964. Studies on the tapeworm Anoplocephala perfoliata (Goeze, 1782). Parasitology, Vol. 54, pp. 451–79.Google Scholar
Lev, R. & Spicer, S. S. 1964. Specific staining of sulphate groups with alcian blue at low pH. J. Histochem. Cytochem., Vol. 12, p. 309.Google Scholar
Levene, C. & Feng, P. 1962. A study of the fixation of the granular elements in rat pancreas. Q. Jl microsc. Sci., Vol. 103, pp. 451–6.Google Scholar
Lewis, P. R. 1958. A simultaneous coupling azo dye technique suitable for whole mounts. Q. Jl microsc. Sci., Vol. 99, pp. 67–71.Google Scholar
Lewis, P. R. 1962. Histochemistry in biology. In Viewpoints in Biology, Vol. 1, pp. 50–89. Ed. J. D. Carthy and C. L. Duddington. London: Butter-worths.Google Scholar
Lison, L. 1936. Histochemie animale. Paris: Gauthier-Villars.Google Scholar
Makhlin, E. E. 1963. Heat resistance of protein complexes of Rana temporaria L. and Rana ridibunda Pall. Problemy Cytoecologii Zhivotnykh, No. 6, pp. 199–207. (In Russian.)Google Scholar
Manwell, C.Southward, E. C. & Southward, A. J. 1966. Preliminary studies on haemoglobin and other proteins of the Pogonophora. J. mar. biol. Ass. U.K., Vol. 46, pp. 115–23.CrossRefGoogle Scholar
Marshall, J. M. & Nachmias, V. T. 1965. Cell surface and pinocytosis. J. Histochem. Cytochem., Vol. 13, pp. 92–104.Google Scholar
Maynard, E. A. 1964. Esterases in crustacean nervous systems. I. Electrophoretic studies on lobsters. J. exp. Zool., Vol. 157, pp. 251–66.Google Scholar
Michel, C. 1964. Histologie, histochimie et innervation de la trompe d'Eulalia viridis (Müller), (polychètes errantes, Phyllodocidae). Bull. Lab. marit. Dinard, T. 49–50, pp. 62–95.Google Scholar
Millot, N. 1948. The histophysiology of the alimentary canal of the earthworm Lumbricus terrestris Linnaeus. I. The process of extrusion from the intestinal glands, and other features of the intestinal epithelium. Proc. R. Soc. B, Vol. 135, pp. 358–81.Google Scholar
Mitchell, P. 1963. Molecule, group and electron translocation through natural membranes. Biochem. Soc. Symp., Vol. 22, pp. 142–68.Google Scholar
Moroney, S. P. & Rankin, R. R. 1953. Cholinesterase and ciliary activity in the gill of Mytilus. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 105, p. 378.Google Scholar
Mowry, R. W. 1963. The special value of methods that colour both acidic and vicinal hydroxyl groups in the histochemical study of mucins. Ann. N. Y. Acad. Sci., Vol. 106, pp. 402–23.Google Scholar
Muller, R. 1965. The histochemical localisation of phosphatases and esterases in Australorbis glabrata. Proc. zool. Soc. Lond., Vol. 144, pp. 229–38.Google Scholar
Myers, D. K. 1960. Carboxyl ester cleavage (survey). In The Enzymes, Vol. 4, pp. 475–483. Ed. P. Boyer, H. Lardy and K. Myrbäck. New York: Academic Press.Google Scholar
Myers, D. K.Schotte, A.Boer, H. & Borsje-Bakker, H. 1955. Studies on aliesterases and other lipid hydrolysing enzymes. 3. Inhibition of esterases of the pancreas. Biochem. J., Vol. 61, pp. 521–8.Google Scholar
Nimitz, M. A. & Giese, A. C. 1964. Histochemical changes correlated with re-productive activity and nutrition in the chiton Katherina tunicata. Q. Jl microsc. Sci., Vol. 105, pp. 481–95.Google Scholar
Nørrevang, A. 1965. Structure and function of the tentacle and pinnules of Siboglinum ekmani Jägersten (Pogonophora). Sarsia, No. 21, pp. 37–47.Google Scholar
Owen, G. 1958. Observations of the stomach and digestive gland of Scutus brevisulcus (Blainville). Proc. malac. Soc. Lond., Vol. 33, pp. 103–14.Google Scholar
Park, K.Williams, W. T.Prescott, J. M. & Hood, D. W. 1962. Amino acids in deep-sea water. Science, Vol. 138, pp. 531–2.Google Scholar
Parry, D. A. 1944. Structure and function of the gut in Spadella cephaloptera and Sagitta setosa. J. mar. biol. Ass. U.K., Vol. 26, pp. 16–36.Google Scholar
Patterson, E. K.Hsiao, S. H. & Keppel, A. 1963. Studies on dipeptidases and aminopeptidases. J. biol. Chem., Vol. 238, pp. 3611–20.Google Scholar
Pearse, A. G. E. 1960. Histochemistry. Theoretical and Applied, 2nd ed. London: Churchill.Google Scholar
Pugh, D. 1963. The cytology of the digestive and salivary glands of the limpet, Patella. Q. Jl microsc. Set., Vol. 104, pp. 23–37.Google Scholar
Richards, A. G. 1951. The Integument of Arthropods. Minneapolis: University of Minnesota Press.Google Scholar
Runham, N. W. 1962. Further investigations on the histochemistry of molluscan chitin. J. Histochem. Cytochem., Vol. 10, p. 504.Google Scholar
Salthouse, T. N. 1962. Histochemistry and staining of chitin. J. Histochem. Cytochem., Vol. 10, pp. 109–10.Google Scholar
Schardein, J. L. & Waitz, J. A. 1965. Histochemical studies of esterases in the cuticle and nerve cords of four cyclophyllidean cestodes. J. Parasitol., Vol. 51, pp. 356–63.Google Scholar
Schulze, P. 1922. Über Beziehungen zwischen pflanzlichen und tierischen Skelettsubstanzen und über Chitinreaktionen. Biol. Zbl., Bd. 42, pp. 388–94.Google Scholar
Sleigh, M. A. 1962. The Biology of Cilia and Flagella. Oxford: Pergamon Press.CrossRefGoogle Scholar
Smith, J. E. 1937. The structure and function of the tube feet in certain echinoderms. J. mar. biol. Ass. U.K., Vol. 22, pp. 345–57.Google Scholar
Southward, A. J. & Southward, E. C. 1963. Notes on the biology of some Pogonophora. J. mar. biol. Ass. U.K., Vol. 43, pp. 57–64.Google Scholar
Southward, E. C. 1959. Two new species of Pogonophora from the north-east Atlantic. J. mar. biol. Ass. U.K., Vol. 38, pp. 439–44.Google Scholar
Southward, E. C. 1963. Pogonophora. Oceanogr. mar. Biol. A. Rev., Vol. 1, pp. 405–28.Google Scholar
Southward, E. C. & Southward, A. J. 1958. On some Pogonophora from the north-east Atlantic, including two new species. J. mar. biol. Ass. U.K., Vol. 37, pp. 627–32.Google Scholar
Stephens, G. C. 1964. Uptake of organic material by aquatic invertebrates. III. Uptake of glycine by brackish water annelids. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 126, pp. 150–62.Google Scholar
Sumner, A. T. 1965. The cytology and histochemistry of the digestive glands of Helix. Q. Jl microsc. Set., Vol. 106, pp. 173–92.Google Scholar
Threadgold, L. T. 1962. An electron microscope study of the tegument and associated structures of Dipylidium caninum. Q.Jl microsc. Sci., Vol. 103, pp. 135–40.Google Scholar
Ushakov, B. 1964. Thermostability of cells and proteins of poikilotherms and its significance in speciation. Physiol. Rev., Vol. 44, pp. 518–60.Google Scholar
Vinogradova, A. N. 1963. Heat resistance and optimal temperature of ATP activity of actomyosin in Carcinus maenas (L.), Hyas araneus hoeki Bir., Raja clavata L. and Raja radiata Donov. from the Black and Barents Seas. Problemy Cytoecologii Zhivotnykh, No. 6, pp. 189–94. (In Russian.)Google Scholar
Vonk, H. J. 1960. Digestion and metabolism. In The Physiology of Crustacea, Vol. 1, pp. 291–316. Ed. T. H. Waterman. New York: Academic Press.Google Scholar
Vovelle, J. 1958. Remarques sur la structure du tube de Sabellaria alveolata (L.) et les formations glandulaires impliquée dans son edification. Archs Zool. exp. gén., T. 95, PP. 52–67.Google Scholar
Wachstein, M.Meisel, E. & Falcon, C. 1961. Histochemistry of thiolacetic acid esterase; a comparison with non-specific esterase with special regard to the effect of fixatives and inhibitors on intracellular localization. J. Histochem. Cytochem., Vol. 9, pp. 325–39.Google Scholar
Webb, M. 1964. The posterior extremity of Siboglinum fiordicum (Pogonophora). Sarsia, No. 15, pp. 33–6.Google Scholar
Webb, M. 1965. Additional notes on the adult and larva of Siboglinum fiordicum and on the possible mode of tube formation. Sarsia, No. 20, pp. 21–34.Google Scholar
Wigglesworth, V. B. 1958. The distribution of esterase in the nervous system and other tissues of the insect Rhodnius prolixus. Q. Jl microsc. Sci., Vol. 99, pp. 441–50.Google Scholar