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Nutritional potentials inZoanthus sociathus (Coelenterata, Anthozoa)
Ernährungsmöglichkeiten beiZoanthus sociatus (Coelenterata, Anthozoa)
Helgoländer wissenschaftliche Meeresuntersuchungen volume 26, pages 174–216 (1974)
Kurzfassung
Die KrustenanemoneZoanthus sociatus (Ellis) lebt in Symbiose mit Dinoflagellaten der GattungGymnodinium. Feinstrukturelle, physiologische und biochemische Aspekte dieser symbiotischen Partnerschaft wurden untersucht.Z. sociatus zeichnet sich durch eine autotrophe Ernährungsweise aus, indem Photosyntheseprodukte der intrazellulär lebenden Zooxanthellen verwertet werden. Darüber hinaus ernährt sichZ. sociatus auch heterotroph durch die Aufnahme von Detritus, Bakterien und gelösten organischen Substanzen. Freiland- und Laboruntersuchungen erbrachten jedoch keine Hinweise, daß lebendes Zooplankton verwertet wird, obgleich in bezug auf das Verhalten gegenüber Nahrungsstoffen, die Ultrastruktur der Mesenterialfilamente und die Art der Verdauung keine wesentlichen Abweichungen gegenüber anderen planktonfressenden Coelenteraten festgestellt werden konnten.Z. sociatus nimmt offensichtlich — ebenso wie andere wirbellose Riffbewohner — eine polytrophe Stellung innerhalb des Ökosystems Korallenriff ein. Die Vielseitigkeit der Ernährungsweise wird unter dem Gesichtspunkt der ökologischen Stabilität des Lebensraumes Korallenriff erörtert.
Summary
1. The tropical coral reef-dwelling coelenterateZoanthus sociatus (Ellis) lives in mutualistic symbiosis with dinoflagellates of the genusGymnodinium. These algae are intracellular.
2. Analysis of the photosynthetic contribution of these endosymbionts shows a direct transfer of photosynthate from algae to animal and utilization of such substances by the animal. Such transfer does not involve destruction of the algae. In vitro studies of the photosynthetic products of the algae show that they synthesize a wide range of metabolites, but selectively release only a few including glycerol, glucose and alanine. These data indicate that such organisms possess an autotrophic mode of nutrition.
3.Z. sociatus shows a well defined feeding behaviour when offered homogenates ofEchinometra eggs. A similar behaviour may be elicited with reduced glutathione. Proline and glycine produced “mouth opening” responses but not the complete feeding response. Alanine, glutamic acid and aspartic acid gave no response.
4. The ultrastructure of the mesenterial filaments shows that the tissue is well differentiated and possesses nematocysts (holotrichous isorhyzas). Several distinct cell types including mucus secreting and “zymogen” cells have been recognized. These cells probably play an important role in extracellular digestion.
5. The rate of digestion of exogenously supplied proteins byZ. sociatus compares favourably with that of sea anemones and corals. Digestion is both extracellular and intracellular, the latter process taking place after particle phagocytosis in the “digestive-excretory” cells of the mesenteries proximal to the filament.
6.Z. sociatus can absorb dissolved amino acids and sugars from very low concentrations (10−6–10−7M), and may incorporate such metabolites particularly into reproductive tissue.
7. The pycnotic zooxanthellae found in the cells of the “digestive-excretory” zone of the mesenteries are probably derived from other areas of the animal gastroderm. These algae appear to undergo senesence in this tissue, but are not digested by the animals. This is very likely a normal phenomenon, in which case the “digestive-excretory” zone of the filament could be regarded as a “grave yard” for old defunct members of the algal population.
8. The polytrophic habit of reef-dwelling invertebrates with photosynthetic endosymbionts is viewed as an important parameter of coral reef nutrition, lending a great deal of nutritional versatility to animals. Such plasticity is probably a reflection of microinstability within an overall stable ecosystem.
Literature cited
Ashworth, J. H., 1898. The stomodaeum and mesenterial filaments ofXenia. Proc. R. Soc. (B)63, 443–446.
—— 1899. The structure ofXenia hicksoni nov. sp. with some observations onHeteroxenia. Q. Jl microsc. Sci.42, 245–304.
Ayala, F. J., Hedgecock, D., Zumwalt, G. S. &Valentine, J. W., 1973. Genetic variation inTridacna maxima, an ecological analog of some unsuccessful evolutionary lineges. Evolution, Lancaster, Pa.27, 177–191.
Boschma, H., 1925a. The nature of the association between Anthozoa and zooxanthellae. Proc. natl Acad. Sci. U.S.A.11, 65–67.
—— 1925b. Feeding reactions and digestion in the coral polypsAstrangia danae with notes on its symbiosis with zooxanthellae. Biol. Bull. mar. biol. Lab., Woods Hole49, 407–439.
—— 1926. On the food of reef corals. Proc. Sect. Sci. K. ned. Acad. Wet.29, 993–997.
Cowie, D. B., Bolton, E. T. &Sands, M. K., 1952. The labelling of bacterial cells with35S for the production of high specific activity compounds. Archs Biochem. Biophys.35, 140–145.
DiSalvo, L. H., 1971a. Ingestion and assimilation of bacteria by two scleractinian coral species. In: Experimental coelenterate biology. Ed. byH. M. Lenhoff, L. Muscatine &L. V. Davis. Univ. of Hawaii Press, Honolulu, 129–136.
—— 1971b. Regenerative functions and microbial ecology of coral reefs: labelled bacteria in a coral reef ecosystem. J. exp. mar. Biol. Ecol.7, 123–136.
Dodge, J. D., 1966. The Dinophyceae. In: The chromosomes of the algae. Ed. byM. B. Godward. Arnold, London, 96–115.
—— 1970. Changes in chloroplast fine structure during the autumnal senescence ofBetula leaves. Ann. Bot.34, 817–824.
—— 1971. Fine structure of the Pyrrophyta. Bot. Rev.37, 481–508.
Droop, M. R., 1963. Algae and invertebrates in symbiosis. Symp. Soc. gen. Microbiol.13, 171–199.
Ellis, J., 1767. An account of theActinia sociata. Phil. Trans. R. Soc.57, 428–437.
Fankbonner, P. V., 1971. Intracellular digestion of symbiotic zooxanthellae by host amoebocytes in giant clams (Bivalvia, Tridacnidae), with a note on the nutritional role of the hypertrophied siphonal epidermis. Biol. Bull. mar. biol. Lab., Woods Hole141, 222–234.
Franker, C. K., 1971. Electrophoretic identity of polypeptides from the nuclear membrane ofAnthropleura — associated zooxanthellae. J. Physcol.7, 20–24.
Fulton, C., 1963. Proline control of the feeding reaction ofCordylophora. J. gen. Physiol.46, 823–837.
Glynn, P. W., 1973. Aspects of the ecology of coral reefs in the Western Atlantic region. In: Biology and geology of coral reefs. Ed. byO. A. Jones &R. Endean. Acad. Press, New York,2, 271–324.
Gohar, H. A., 1940. Studies on the Xeniidae of the Red Sea. Publs mar. biol. Stn. Ghardaqa2, 25–118.
—— 1948. A description and some biological studies of a new alcyonarian speciesClavularia hamra Gohar. Publs mar. biol. Stn. Ghardaqa6, 3–33.
Gomori, G., 1950. An improved histochemical technique for acid phosphatase. Stain Technol.25, 81–85.
Goreau, T. F., 1959. The ecology of Jamaican coral reefs. I. Species composition and zonation. Ecology40, 69–90.
—— 1961. Problems of growth and calcium deposition in reef corals. Endeavour20, 32–40.
—— 1963. Calcium carbonate deposition by coralline algae and hermatypic corals in relation to their roles as reef builders. Ann. N. Y. Acad. Sci.109, 127–167.
—— 1964. Mass expulsion of zooxanthellae from Jamaican reef communities after hurricane Flora. Science N. Y.145, 383–386.
—— &Hartman, W. D., 1963. Boring sponges as controlling factors in the formation and maintenance of coral reefs. In: Mechanisms of hand tissue destruction. Ed. byR. F. Sognnaes. Am. Ass. for the Advancement of Science, Washington, 25–54.
—— &Philpott, D. E., 1956. Electron micrographic studies of flagellated epithelia in madreporarian corals. Expl Cell Res.10, 552–556.
—— &Yonge, C. M., 1971. Reef corals: Autotrophs or heterothrops? Biol. Bull. mar. biol. Lab., Woods Hole141, 247–260.
—— 1973. On utilization of photosynthetic products from zooxanthellae and of dissolved amino acids inTridacna maxima f.elongata (Roeding). J. Zool., Lond.169, 417–454.
Grassle, J. F., 1973. Variety in coral reef communities. In: Biology and geology of coral reefs. Ed. byO. A. Jones &R. Endean. Acad. Press, New York,2, 247–270.
Greene, R. W., 1970. Symbiosis in sacoglossan opisthobranchs: translocation of photosynthetic products from chloroplasts to host tissue. Malacologia10, 369–380.
——, 1972. Symbiosis in sacoglossan opisthobranchs: photosynthetic products of animal-chloroplast associations. Mar. Biol.14, 253–259.
Hadden, E. M., 1968. The relationship betweenZoanthus sociatus and its zooxanthellae. Ph. D. Diss. Yale Univ., 104 pp.
Heberts, C., 1970. Note sur un zoanthaine de la cote sudouest de madagascar. Recl. Trav. Stn. mar. Endoume10, 305–315.
Hessler, R. R. &Sanders, H. L., 1967. Faunal diversity in the deep sea. Deep Sea Res.14, 65–78.
Holt, C. von, 1968. Uptake of glycine and release of nucleoside polyphosphates by zooxanthellae. Comp. Biochem. Physiol.26, 1071–1079.
—— &Holt, M. von, 1968a. Transfer of photosynthetic products from zooxanthellae to coelenterates hosts. Comp. Biochem. Physiol.24, 73–81.
—— 1968b. The secretion of organic compounds by zooxanthellae isolated from various types ofZoanthus. Comp. Biochem. Physiol.24, 83–92.
Johannes, R. W., 1967. Ecology of organic aggregates in the vicinity of a coral reef. Limnol. Oceanogr.12, 189–195.
—— &Kuenzel, N. T., 1970. The role of zooplankton in the nutrition of some scleractinian corals. Limnol. Oceanogr.15, 579–586.
Kanwisher, J. W. &Wainwright, S. A., 1967. Oxygen balance in some reef corals. Biol. Bull. mar. biol. Lab., Woods Hole133, 378–390.
Kay, D. H., 1965. Techniques for electron microscopy. Davis, Philadelphia, Penn., 560 pp.
Kevin, M., Hall, W. T., McLaughlin, J. J. &Zahl, P. A., 1969.Symbiodinium microadriaticum Freudenthal, a revised taxonomic description, ultrastructure. J. Phycol.5, 341–350.
Lang, J. C., 1973. Interspecific aggression by scleractinian corals. II. Why the race is not only to the swift. Bull. mar. Sci.23, 260–279.
Lehman, J. T. &Porter, J. W., 1973. Chemical activation of feeding in the caribbean reef-building coralMontastrea cavernosa. Biol. Bull. mar. biol. Lab., Woods Hole145, 140–149.
Lenhoff, H. M., 1968a. Chemical perspectives on the feeding response, digestion and nutrition of selected coelenterates. In: Chemical zoology. Ed. byM. Florkin &B. Scheer. Acad. Press, New York,2, 157–221.
—— 1968b. Behavior, hormones and hydra. Science, N. Y.166, 434–442.
Lewis, D. H. &Smith, D. C., 1971. The autotrophic nutrition of symbiotic marine coelenterates with special reference to hermatypic corals. I. Movement of photosynthetic products between the symbionts. Proc. R. Soc. (B)178, 111–129.
Lindstedt, K. J., 1971. Chemical control of feeding behavior. Comp. Biochem. Physiol.39A, 553–581.
Lowry, O. H., Rosebrough, N. J., Farr, A. L. &Randall, R. J., 1951. Protein measurement with the Folin phenol reagent. J. biol. Chem.193, 265–275.
McLaughlin, J. J. &Zahl, P. A., 1966. Endozoic algae. In: Symbiosis. Ed. byS. M. Henry. Acad. Press, New York,1, 257–297.
Mariscal, R. N. &Lenhoff, H. M., 1968. The chemical control of feeding behavior inCyphastrea ocellina and some other Hawaiian corals. J. exp. Biol.49, 689–699.
Murdock, G. R. &Lenhoff, H. M., 1968. Alcohol soluble proteins: their formation and assimilation during intracellular digestion inHydra littoralia andAiptasia sp. Comp. Biochem. Physiol.26, 963–970.
Muscatine, L., 1967. Glycerol excretion by symbiotic algae from corals andTridacna and its control by the host. Science, N. Y.156, 516–519.
—— 1971. Endosymbiosis of algae and coelenterates. In: Experimental coelenterate biology. Ed. byH. M. Lenhoff, L. Muscatine &L. V. Davis. Univ. of Hawaii Press, Honolulu, 179–191.
—— 1973. Nutrition of corals. In: Biology and geology of coral reefs. Ed. byO. A. Jones &R. Endean. Acad. Press, New York, 77–115.
—— &Cernichiari, E., 1969. Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull. mar. biol. Lab., Woods Hole137, 506–523.
—— &Carnichiari, E., 1972. Some factors influencing selective release of soluble organic material by zooxanthellae from reef corals. Mar. Biol.13, 298–308.
Nicol, J. A., 1959. Digestion in sea anemones. J. mar. biol. Ass. U.K.38, 469–476.
Odum, H. T. &Odum, E. P., 1956. Corals as producers, herbivores, carnivores and possible decomposers. Ecology37, 385.
Pardy, R. L. &Muscatine, L., 1973. Recognition of symbiotic algae byHydra viridis. A quantitative study of the uptake of living algae by aposymbioticH. viridis. Biol. Bull. mar. biol. Lab., Woods Hole145, 565–579.
Porter, J. W., 1973. Zooplankton feeding by the Caribbean reef-building coralMontastrea cavernosa. Second international symposium on coral reefs. (in press).
Powell, J. R., 1971. Genetic polymorphism in varied environments. Science, N.Y.,174, 1035–1036.
Pütter, A., 1909. Die Ernährung der Wassertiere und der Stoffhaushalt der Gewässer. Fischer, Jena, 168 pp.
Ramsey, J. A., 1971. Insect rectum. Phil. Trans. R. Soc. (B)262, 251–260.
Reimer, A. A., 1971a. Chemical control of feeding behavior and role of glycine in the nutrition ofZoanthus (Coelenterate, Zoanthidea). Comp. Biochem. Physiol.39A, 743–759.
—— 1971b. Feeding behavior in the Hawaiian ZoanthidsPolythoa andZoanthus. Pacif. Sci.25, 512–520.
Roffman, B., 1968. Patterns of oxygen exchange in some Pacific corals. Comp. Biochem. Physiol.27, 405–418.
Rogers, A. W., 1969. Techniques of autoradiography. Elsevier, Amsterdam, 338 pp.
Sanders, H. L., 1969. Benthic marine diversity and the time stability hypothesis. Brookhaven Symp. Biol.22, 71–80.
Schmitter, R. E., 1971. The fine structure ofGonyanlax polyedra, a bioluminescent marine dinoflagellate. J. Cell Sci.9, 147–173.
Slobodkin, L. B. &Sanders, H. L., 1969. On the contribution of environmental predictability to species diversity. Brookhaven Symp. Biol.22, 82–93.
Smith, D. C., Muscatine, L. &Lewis, D. H., 1969. Carbohydrate movement from autotrophs to heterotrophs in parasitic and mutualistic symbiosis. Biol. Rev.44, 17–90.
Schlichter, D., 1973. Ernährungsphysiologische und ökologische Aspekte der Aufnahme in Meerwasser gelöster Aminosären durchAnemonia sulcata (Coelenterata, Anthozoa). Oecologia11, 315–350.
Sorokin, Y. I., 1973. Microbial aspects of the productivity of coral reefs. In: Biology and geology of coral reefs. Ed. byO. A. Jones &R. Endean. Acad. Press, New York2, 17–45.
Stephens, G. C., 1967. Dissolved organic material as a nutritional source for marine and estuarine invertebrates. In: Estuaries. Ed. byG. H. Lauff. Am. Ass. for the Advancement of Science, Washington, 367–373.
—— 1968. Dissolved organic matter as a potential source of nutrition for marine animals. Am. Zool.8, 95–106.
Taylor, D. L., 1968. In situ studies on the cytochemistry and ultrastructure of a symbiotic marine dinoflagellate. J. mar. biol. Ass. U.K.48, 349–366.
—— 1969a. The nutritional relationship ofAnemonia sulcata (Pennant) and its dinoflagellate symbiont. J. Cell Sci.4, 751–762.
Taylor, D. L. 1969b. On the regulation and maintenance of algal numbers in zooxanthellae — coelenterate symbiosis. J. mar. biol. Ass. U.K.49, 1057–1065.
—— 1969c. Identity of zooxanthellae isolated from Pacific Tridacnidae. J. Phycol.5, 336–340.
—— 1973. Symbiotic pathway of carbon in coral reef ecosystems. Present status and future prospects. Helgoländer wiss. Meeresunters.24, 276–283.
-- 1974. Nutrition of algal-invertebrate symbiosis. I. Utilization of soluble organic nutrients by symbiont free hosts. (In press).
Trench, R. K., 1969. The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. Ph. D. Diss. Univ. of California, Los Angeles, 140 pp.
—— 1970. Synthesis of a mucous cuticle by a zoanthid. Nature, Lond.227, 1155–1156.
—— 1971a. The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. I. The assimilation of photosynthetic products of zooxanthellae by two marine coelenterates. Proc. R. Soc. (B)177, 225–235.
—— 1971b. The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. II. Liberation of fiexed14C by zooxanthellaein vitro. Proc. R. Soc. (B)177, 237–250.
—— 1971c. The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. III. The effect of homogenates of host tissues on the excretion of photosynthetic productsin vitro by zooxanthellae from two marine coelenterates. Proc. R. Soc. (B)177, 251–264.
—— 1973. Further studies on the mucopolysaccharide secreted by the pedal gland of the marine slugTridachia crispata (Opisthobranchia, Sacoglossa). Bull. mar. Sci.23, 299–312.
—— &Gooday, G. W., 1973. Incorporating of3H-leucine into protein by animal tissues and by endosymbiotic chloroplasts inElysia viridis Montagu. Comp. Biochem. Physiol.44A, 321–330.
—— &Smith, D. C., 1973. The association between chloroplasts ofCodium fragile and the molluscElysia viridis. II. Chloroplast ultrastructure and photosynthetic carbon fixation inE. viridis. Proc. R. Soc. (B)184, 63–81.
—— —— —— 1974. The association between chloroplasts ofCodium fragile and the molluscElysia viridis. III. Movement of photosynthetically fixed14C in tissues of intact livingE. viridis and inTridachia crispata. Proc. R. Soc. (B)185, 453–464.
—— &Bystrom, B. G., 1969. Chloroplasts as functional organelles in animal tissues. J. Cell Biol.42, 404–417.
—— &Muscatine, L., 1970. Utilization of photosynthetic products of symbiotic chloroplasts in mucus synthesis byPlacobranchus ianthobapsus (Gould) (Opisthobranchia, Sacoglossa). Comp. Biochem. Physiol.37, 113–117.
—— —— —— 1972. Symbiotic chloroplasts: their photosynthetic products and contribution to mucus synthesis in two marine slugs. Biol. Bull. mar. biol. Lab., Woods Hole142, 335–349.
Vandermulen, J. H., 1972. Studies on skeleton formation, tissue ultrastructure and physiology of calcification in the reef coralPocillopora damicornis (L.). Ph. D. Diss. Univ. of California, Los Angeles, 236 pp.
—— &Muscatine, L., 1972. The effect of inhibitors of photosynthesis on zooxanthellae in corals and other marine invertebrates. Mar. Biol.16, 185–191.
Yonge, C. M., 1931. Studies on the physiology of corals. III. Assimilation and excretion. Scient. Rep. Gt. Barrier Reef Exped.1, 83–91.
—— 1940. The biology of reef-building corals. Scient. Rep. Gr. Barrier Reef Exped.1, 353–391.
—— 1968. Living corals. Proc. R. Soc. (B)169, 209–260.
—— 1973. The nature of reef-building (hermatypic) corals. Bull. mar. Sci.23, 1–15.
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Contribution No. 601 from the Bermuda Biological Station for Research, Inc. St. Georges West, Bermuda.
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Trench, R.K. Nutritional potentials inZoanthus sociathus (Coelenterata, Anthozoa). Helgolander Wiss. Meeresunters 26, 174–216 (1974). https://doi.org/10.1007/BF01611382
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DOI: https://doi.org/10.1007/BF01611382