Hostname: page-component-7c8c6479df-hgkh8 Total loading time: 0 Render date: 2024-03-27T16:01:46.845Z Has data issue: false hasContentIssue false

Acidic allomones in marine organisms

Published online by Cambridge University Press:  11 May 2009

T. E. Thompson
Affiliation:
Department of Zoology, University of Bristol, Woodland Road, Bristol BS8 1UG

Extract

The phenomenon of acid secretion has arisen independently many times, for feeding, for penetrating calcareous material to make a shelter or to pursue prey, or for defence. This last category contains examples from many groups of marine organisms, in which acidic allomones may serve to deter fouling by epibionts or predation by teleost fish. Histochemical and histophysical methods have increased the precision with which acidic allomones can be identified within acid vacuoles, cells, glands, sacs or capsules. Acidic allomones are produced in pleurobranch molluscs by unicellular epidermal glands, by multicellular subepidermal sacs, or by an arborescent internal acid gland, connected to the buccal mass by a thick medio-dorsal duct. Some species have all three types. In the case of the epidermis, discharge is probably triggered directly by the trauma of attack by a predator (effectively, holocrine discharge), but the other types of gland are discharged by contraction of a strong muscle sheath, without tissue damage. Cypraeid molluscs have extensive, mobile mantle lobes which can ensheath the massive shell temporarily. The epidermal acid glands are orientated within the mantle so as to discharge away from the shell. The lamellariid and philinid molluscs have internal shells, well protected from chemical attack, and the multicellular, subepidermal acid glands are situated over all the surfaces of the body. In the tunicates investigated, both blood and tunic were neutral in Ciona intestinalis, but they were both acid (pH 1) in Ascidiella aspersa. In Ascidiella scabra and Ascidia mentula the blood was neutral, and the tunic alone was acid. The acid tunics contained abundant blind lacunae. It is unlikely that these acid-filled lacunae correspond to the blind-ending arterial ampullae described by other workers. Discharge is probably brought about directly through the trauma of attack. The perennial species of the alga Desmarestia, D. aculeata, exhibited a pH near to neutrality. Two annual species, D. dresnayi and D. ligulata, contained acid of pH 1–2, and showed strong precipitation of BaSO4 after BaCl2 treatment. Sections confirmed that the acid is normally held within the swollen parenchymatous cells which pack the sporophyte frond. The cuticle is comparatively thin in the acidic species. In conclusion, it is argued that acid secretion may be the allelochemical analogue of warning or aposematic coloration.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1988

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

REFERENCES

Bateson, W., 1890. The sense-organs and perceptions of fishes; with remarks on the supply of bait. Journal of the Marine Biological Association of the United Kingdom, 1, 225256.Google Scholar
Carriker, M. R., 1969. Excavation of boreholes by the gastropod, Urosalpinx: an analysis by light and scanning electron microscopy. American Zoologist, 9, 917933.Google Scholar
Day, J. A., 1969. Feeding of the cymatiid gastropod, Argobuccinum argus, in relation to the structure of the proboscis and secretions of the proboscis gland. American Zoologist, 9, 909916.Google Scholar
Dorsett, D. A., 1961. The behaviour of Polydora ciliata (Johnst.). Tube building and burrowing. Journal of the Marine Biological Association of the United Kingdom, 41, 577590.CrossRefGoogle Scholar
Edmunds, M., 1968. Acid secretion in some species of Doridacea (Mollusca, Nudibranchia). Proceedings of the Malacological Society of London, 38, 121133.Google Scholar
Endean, R., 1953. Discovery of iron in tunicin-forming blood cells of an ascidian. Nature, London, 172, 123.CrossRefGoogle ScholarPubMed
Endean, R., 1961. The test of the ascidian, Phallusia mammillata. Quarterly Journal of Microscopical Science, 102, 107117.Google Scholar
Eppley, R. W. & Bovell, C. R., 1958. Sulfuric acid in Desmarestia. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 115, 101106.Google Scholar
Fange, R. & Lidman, U., 1976. Secretion of sulfuric acid in Cassidaria echinophora Lamarck (Mollusca: Mesogastropoda, marine carnivorous snail). Comparative Biochemistry and Physiology, 53 A, 101103.Google Scholar
Fontaine, A. R., 1964. The integumentary mucous secretions of the ophiuroid Ophiocomina nigra. Journal of the Marine Biological Association of the United Kingdom, 44, 145—162.CrossRefGoogle Scholar
Garstang, W., 1890. A complete list of the opisthobranchiate Mollusca found at Plymouth; with further observations on their morphology, colours, and natural history. Journal of the Marine Biological Association of the United Kingdom, 1, 399—457.Google Scholar
Goodbody, I., 1974. The physiology of ascidians. Advances in Marine Biology, 12, 2149.Google Scholar
Hawkins, C. J., James, G. A., Parry, D. L. & Swinehart, J. H., 1983. Intracellular acidity in the ascidian. Comparative Biochemistry and Physiology, 76 B, 559565.Google Scholar
Henze, M., 1911. Untersuchungen über das Blut der Ascidien. I. Mitteilung. Die Vanadiumverbindung der Blutkörperchen. Hoppe-Seyler's Zeitschrift für physiologische Chemie, 72, 494501.Google Scholar
Henze, M., 1913. Untersuchungen über das Blut der Ascidien. III. Mitteilung. Hoppe-Seyler's Zeitschrift für physiologische Chemie, 86, 340344.Google Scholar
Hodgkin, N. M., 1962. Limestone boring by the mytilid Lithophaga. Veliger, 4, 123129.Google Scholar
Houbrick, J. R. & Fretter, V., 1969. Some aspects of the functional anatomy and biology of Cymatium and Bursa. Proceedings of the Malacological Society of London, 38, 415429.Google Scholar
Hughes, R. N. & Hughes, H. P. I., 1981. Morphological and behavioural aspects of feeding in the Cassidae (Tonnacea, Mesogastropoda). Malacologia, 20, 385402.Google Scholar
Johnson, E. L., 1982. Modern ion chromatography. International Laboratory, 14, 110115.Google Scholar
Kniffen, J. C., 1968. Acid secretion in Cypraea. American Journal of Digestive Diseases, 13, 775778.Google Scholar
Marbach, A. & Tsurnamal, M., 1973. The biology of Berthellina citrina (Gastropoda: Opisthobranchia) and its defensive acid secretion. Marine Biology, 21, 331339.Google Scholar
Panceri, P., 1869. Gli organi e la secrezione dell'acido solforico nei gasteropodi. Atti dell'Accademia delle scienze fisiche e matematiche, 4, 56 pp.Google Scholar
Parry, D. L., 1984. Chemical properties of the test of ascidians in relation to predation. Marine Ecology -Progress Series, 17, 279282.CrossRefGoogle Scholar
Pirie, B. J. S. & Bell, M. V., 1984. The localization of inorganic elements, particularly vanadium and sulphur, in haemolymph from the ascidians Ascidia mentula (Müller) and Ascidiella aspersa (Müller). Journal of Experimental Marine Biology and Ecology, 74, 187194.CrossRefGoogle Scholar
Preyer, W., 1866. Uber das für speichel gehaltene sekret von Dolium galea. Sitzungsberichte der niederrhein Gesellschaft für Natur- und Heilkunde zu Bonn, 1866, 69.Google Scholar
Schulz, F. N., 1905. Der histologische Bau der Sauredrüse von Pleurobranchaea Meckelii. Verhandlungen der Gesellschaft deutscher Naturforscher und Ärzte. Leipzig. 76, 487—489.Google Scholar
Smith, M., 1970. The blood cells and tunic of the ascidian Halocynthia aurantium (Pallas). I. Hematology, tunic morphology and partition of cells between blood and tunic. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 138, 354378.Google Scholar
Steedman, H. F., 1950. Alcian blue 8 GS: a new stain for mucin. Quarterly Journal of Microscopical Science, 91, 477479.Google Scholar
Steedman, H. F., 1970. A one-solution triacid general stain which differentiates oxygenated from non-oxygenated red blood corpuscles. Stain Technology, 45, 247253.Google Scholar
Stoecker, D., 1978. Resistance of a tunicate to fouling. Biological Bulletin, Marine Biological Laboratory, Woods Hole, Mass., 155, 615626.Google Scholar
Stoecker, D., 1980. Chemical defenses of ascidians against predators. Ecology, 61, 13271334.Google Scholar
Thompson, T. E., 1960 a. Defensive acid secretion in marine gastropods. Journal of the Marine Biological Association of the United Kingdom, 39, 115122.CrossRefGoogle Scholar
Thompson, T. E., 1960 b. Defensive adaptations in opisthobranchs. Journal of the Marine Biological Association of the United Kingdom, 39, 123134.CrossRefGoogle Scholar
Thompson, T. E., 1961. Acid-secretion in British cowries. Proceedings of the Malacological Society of London, 34,210211.Google Scholar
Thompson, T. E., 1965. Epidermal acid secretion in some marine polyclad Turbellaria. Nature, London, 206, 954955.Google Scholar
Thompson, T. E., 1969. Acid secretion in Pacific Ocean gastropods. Australian Journal of Zoology, 17, 755764.Google Scholar
Thompson, T. E., 1976. Biology of Opisthobranch Molluscs, vol. I. London: Ray Society.Google Scholar
Thompson, T. E., 1983. Detection of epithelial acid secretions in marine molluscs: review of techniques, and new analytical methods. Comparative Biochemistry and Physiology, 74 A, 615621.CrossRefGoogle Scholar
Thompson, T. E., 1986. Investigation of the acidic allomone of the gastropod mollusc Philine aperta by means of ion chromatography and histochemical localisation of sulphate and chloride ions. Journal of Molluscan Studies, 52, 3844.Google Scholar
Thompson, T. E. & Colman, J. G., 1984. Histology of acid glands in Pleurobranchomorpha. Journal of Molluscan Studies, 50, 6667.Google Scholar
Thompson, T. E. & Gathercole, L. J., 1986. Histophysical demonstration of barium sulphate in acidic epithelia of molluscs and other organisms following irrigation in vivo with aqueous barium chloride. Journal of Molluscan Studies, 52, 261262.CrossRefGoogle Scholar
Troschel, F. H., 1854. Ueber den Speichel von Dolium galea Lam. Akademie der Wissenschaften zu Berlin, 1854, 486494.CrossRefGoogle Scholar
Webb, D. A., 1939. Observations on the blood of certain ascidians, with special reference to the biochemistry of vanadium. Journal of Experimental Biology, 16, 499523.CrossRefGoogle Scholar
Wirth, W. E. & Rigg, G. B., 1937. The acidity of the juice of Desmarestia. American Journal of Botany, 24, 6870.Google Scholar
Yonge, C. M., 1949. The Sea Shore. London: Collins.Google Scholar
Yonge, C. M., 1955. Adaptation to rock boring in Botula and Lithophaga. Quarterly Journal of Microscopical Science, 96, 383—410.Google Scholar
Zottoli, R. A. & Carriker, M. R., 1974. Burrow morphology, tube formation, and microarchitecture of shell dissolution by the spionid polychaete Polydora websteri. Marine Biology, 27, 307316.CrossRefGoogle Scholar