Skip to main content
Log in

Histological studies on Halicryptus spinulosus (Priapulida) with regard to environmental hydrogen sulfide resistance

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The priapulid Halicryptus spinulosus has an outstanding resistance to anoxia and hydrogen sulfide, which enables the animal to survive in deteriorating environments. Whole-body staining procedures, as well as light and scanning electron microscopy were used to study structures and mechanisms possibly involved in sulfide detoxification.

The cuticle of the trunk is covered by a coat of mucus and bacteria. Within this coat considerable amounts of finely dispersed iron are precipitated, probably as a Fe2+-compound. It is suggested that the iron functions as a rechargeable buffer against hydrogen sulfide, protecting both the bacteria and the priapulid host. Although this chemical shield may not alone account for long-term protection, it allows the animal to gain time for metabolic adaptations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Apel, W., 1885. Beitrag zur Anatomic and Histologic des Priapulus caudatus (Lam.) and des Halicryptus spinulosus (v. Sieb.). Z. wiss. Zool. 42: 459–528.

    Google Scholar 

  • Back, H. & F. Prosi, 1985. Distribution of inorganic cations in Limnodrilus udekemianus (Oligochaeta, Tubificidae) using laser induced microprobe mass analysis, with special emphasis on heavy metals. Micron. Mirosc. Acta 16: 145–150.

    Google Scholar 

  • Bagarinao, T. & R. D. Vetter, 1989. Sulfide tolerance and detoxification in shallow-water marine fishes. Mar. Biol. 103: 291–302.

    Google Scholar 

  • Barnes, R. D., 1974. Invertebrate Zoology. 3rd edn. Saunders, Philadelphia etc.

    Google Scholar 

  • Bernárt, I., 1981. Eisenstoffwechsel. G. Fischer Verlag, Stuttgart, New York.

    Google Scholar 

  • Boeck, P., 1984. Der Semidünnschnitt. J. F. Bergmann Verlag München.

  • Brock, T. D., S. W. Smith & M. T. Madigan, 1984. Biology of microorganisms. 4th edn., Prentice Hall, New Jersey.

    Google Scholar 

  • Cavanaugh, C. M., 1983. Symbiotic chemoautotrophic bacteria in sulfide-habitat marine invertebrates. Nature 302: 59–61.

    Google Scholar 

  • Cavanaugh, C. M., S. L. Gardiner, M. L. Jones, H. W. Jannasch & J. B. Waterbury, 1981. Prokaryotic cells in the hydrothermal vent tube worm, Riftia pachyptila Jones: Possible chemoautotrophic symbionts. Science 213: 340–342.

    Google Scholar 

  • Cheng, K. J., R. T. Irvin & J. W. Costerton, 1981. Autochthonous and pathogenic colonization of animal tissues by bacteria. Can. J. Microbiol. 27: 461–490.

    PubMed  Google Scholar 

  • Chia, F.-S. & R. M. Warwick, 1969. Assimilation of labelled glucose from seawater by marine nematodes. Nature 224: 720–721.

    Google Scholar 

  • Daniels, L., N. Belay, B. S. Rajagopal & P. J. Welmer, 1987. Bacterial methanogenesis and growth from CO2 with elemental iron as the sole source of electrons. Science 237: 509–511.

    Google Scholar 

  • Felbeck, H., 1983. Sulfide oxidation and carbon fixation by the gutless clam Solemya reidi: An animal-bacteria symbiosis. J. Comp. Physiol. 152: 3–11.

    Google Scholar 

  • Fischer, E. & I. Horváth, 1977. Cytochemical studies on the cuticle and epidermis of Tubifex tubifex Müll. with special regard to the localization of polysaccharides, heavy metals and the DAB-reactivity. Histochemistry 54: 259–271.

    PubMed  Google Scholar 

  • Fleming, T. P. & K. S. Richards, 1982. Uptake and surface adsorption of zinc by the freshwater tubificid oligochaete Tubifex tubifex. Comp. Biochem. Physiol. 71C: 69–75.

    Google Scholar 

  • Frank, L. & D. Massaro, 1980. Oxygen toxicity. Am. J. Med. 69: 117–126.

    PubMed  Google Scholar 

  • Gibbs, P. E., G. W. Bryan & K. P. Ryan, 1981. Copper accumulation by the Polychaete Melinna palmata: an antipredation mechanism? J. mar. Biol. Ass. U.K. 61: 707–722.

    Google Scholar 

  • Giere, O., B. Rhode & N. Dubilier, 1988. Structural peculiarities of the body wall of Tubificoides benedii (Oligochaeta) and possible relations to its life in sulphidic sediments. Zoomorphology 108: 29–39.

    Google Scholar 

  • Halliwell, B. & J. M. C. Gutteridge, 1985. Free radicals in biology and medicine. Clarendon Press, Oxford.

    Google Scholar 

  • Holland, N. D. & K. H. Nealson, 1978. The fine structure of the Echinoderm cuticle and the subcuticular bacteria of Echinoderms. Acta zool. (Storch.) 59: 169–185.

    Google Scholar 

  • Janssen, H. H., 1989. Heavy metal analysis in earthworms from an abandoned mining area. Zool. Anz. 222: 335–360.

    Google Scholar 

  • Janssen, H. H. & U. Ertelt-Janssen, 1983. Cytochemical demonstration of cadmium and iron in experimental Mytilus edulis. Mikroskopie (Wien) 40: 329–340.

    Google Scholar 

  • Land, J. van der, 1970. Systematics, zoogeography, and ecology of the Priapulida. Zool. Verh. Leiden 112: 1–118.

    Google Scholar 

  • Lojda, Z., R. Gorsrau & T. H. Schiebler, 1976. Enzymhistochemische Methoden. Springer Verlag, Berlin.

    Google Scholar 

  • Millero, F., 1986. The thermodynamics and kinetics of the hydrogen sulfide system in natural waters. Mar. Chem. 18: 121–147.

    Google Scholar 

  • Morill, A. C., E. N. Powell, R. R. Bidigare & J. M. Shick, 1988. Adaptations to life in the sulfide system: a comparison of oxygen detoxifying enzymes in thiobiotic and oxybiotic meiofauna (and freshwater planarians). J. Comp. Physiol. B 158: 335–344.

    Google Scholar 

  • National Research Council, Committee on Medical and Biological Effects of Environmental Pollutants, Subcommittee on Hydrogen Sulfide, 1979. Hydrogen sulfide, University Park Press, Baltimore.

    Google Scholar 

  • Oeschger, R., 1990. Long-term anaerobiosis in sublittoral marine invertebrates from the Western Baltic Sea: Halicryptus spinulosus (Priapulida), Astarte borealis and Arctica islandica (Bivalvia). Mar. Ecol. Prog. Ser. 59: 133–143.

    Google Scholar 

  • Oeschger, R. & R. Schmaljohann, 1988. Association of various types of epibacteria with Halicryptus spinulosus (Priapulida). Mar. Ecol. Progr. Ser. 48: 285–293.

    Google Scholar 

  • Oeschger, R. & H. Theede, 1988. Use of biochemical features of macrobenthic species as indicators of long-term oxygen deficiency. Kiefer Meeresforsch., Sonderh. 6: 99–110.

    Google Scholar 

  • Owen, G., 1965. Observations on the stomach and digestive diverticula of the Lamellibranchiata. II. The nuculidae. Quart. J. Microscop. Sci. 97: 541–567.

    Google Scholar 

  • Owen, G., 1973. The fine structure and histochemistry of the digestive diverticula of the protobranchiate bivalve Nucula sulcata. Phil. Trans. R. Soc., Lond. 183 (B): 249–264.

    Google Scholar 

  • Pearse, A. G. E., 1960. Histochemistry. Theoretical and applied. 2nd edn. London, Churchill.

  • Powell, M. A. & A. J. Arp, 1989. Hydrogen sulfide oxidation by abundant nonhemoglobin heme compounds in marine invertebrates from sulfide-rich habitats. J. exp. Zool. 249: 121–132.

    Google Scholar 

  • Reinheimer, G., 1981. Mikrobiologie der Gewässer. G. Fischer Verlag, Stuttgart.

    Google Scholar 

  • Riemann, F. & M. Schrage, 1988. Carbon dioxide as an attractant for the free-living marine nematode Adoncholaimus thalassophygas. Mar. Biol. 98: 81–85.

    Google Scholar 

  • Rosenberg, L., 1971. Chemical Basis for the histological use of Safranin O in the study of articular cartilage. J. Bone Joint Surgery 53A: 69–82.

    Google Scholar 

  • Schreiber, A., V. Storch, M. Powilleit & R. P. Higgins, 1991. The blood of Halicryptus spinulosus (Priapulida). Can. J. Zool.: in press.

  • Southward, A. J. & E. C. Southward, 1968. On a wholeanimal method for the histochemical localization of enzymes under field conditions. J. mar. biol. Ass. U.K. 48: 323–334.

    Google Scholar 

  • Storch, V., 1991. Priapulida. In: Harrison, F. H. (ed.) Microscopic anatomy of invertebrates, Vol. IV. Liss, New York: in press.

    Google Scholar 

  • Storch, V., R. P. Higgins, Morse, 1989. Internal anatomy of Meiopriapulus fijiensis (Priapulida). Trans. am. Microsc. Soc. 108: 245–261.

    Google Scholar 

  • Theede, H., A. Ponat, K. Hiroki & C. Schlieper, 1969. Studies on the resistance of marine bottom invertebrates to oxygen deficiency and hydrogen sulphide. Mar. Biol. 2: 325–337.

    Google Scholar 

  • Vetter, R. D., 1985. Elemental sulfur in the gills of three species of clams containing chemoautotrophic symbiotic bacteria: A possible inorganic energy storage compound. Mar. Biol. 88: 33–42.

    Google Scholar 

  • Weber, R. E., R. Fange & K. Krogh Rasmussen, 1979. Respiratory significance of priapulid hemerythrin. Mar. Biol. Let. 1: 87–97.

    Google Scholar 

  • Whitten, B. K. & C. J. Goodnight, 1966. Strontium-89 and calcium-45 accumulation in an aquatic oligochaete. Am. Soc. Zool. 6: 508.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Contribution No. 289 of the Alfred-Wegener-Institut für Polar- and Meeresforschung (AWI Bremerhaven).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oeschger, R., Janssen, H.H. Histological studies on Halicryptus spinulosus (Priapulida) with regard to environmental hydrogen sulfide resistance. Hydrobiologia 222, 1–12 (1991). https://doi.org/10.1007/BF00017494

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00017494

Key words

Navigation