Skip to main content
  • Visiting Scientists at the Biologische Anstalt Helgoland (History and Specific Results)
  • Published:

Induction and regulation of metamorphosis in planktonic larvae:Phoronis mülleri (Tentaculata) as archetype

Abstract

The larvae ofPhoronis mülleri are comprised of many diverse behavioural forms that can be manipulated experimentally to facilitate precise assertions about the induction of metamorphosis. Various parameters for inducing metamorphosis as exemplified inPhoronis, such as species-specific substrate, bacteria, the cations Rb+, Cs+ and Hg2+ and tensides, are considered, and their ecologic relevance to natural factors in the sea is demonstrated. Findings on metamorphosis in other marine larvae are summarized. The function of marine bacteria as “ecological ushers” is particularly emphasized.

Literature Cited

  • Barnes, J. R. & Gonor, J. J., 1973. The larval settling response of the lined chitonTonicella lineata. —Mar. Biol.20, 259–264.

    Google Scholar 

  • Barnes, J. R. & Powell, H. T., 1950. Some observations on the effect of fibrous glass surfaces upon the settlement of certain sedentary marine organisms. — J. mar. biol. Ass. U.K.29, 299–302.

    Google Scholar 

  • Bayne, B. L., 1965. Growth and delay of metamorphosis of the larvae ofMytilus edulis. — Ophelia2, 1–47.

    Google Scholar 

  • Bayne, B. L., 1969. The gregarious behaviour of the larvae ofOstrea edulis at settlement. — J. mar. biol. Ass. U.K.49, 327–356.

    Google Scholar 

  • Berking, S., 1988. Ammonia, tetraethylammonium, barium and amiloride induce metamorphosis in the marine hydroidHydractinia. — Wilhelm Roux Arch. dev. Biol.197, 1–9.

    Google Scholar 

  • Berrill, N. J., 1947. The development and growth ofCiona. — J. mar. biol. Ass. U.K.26, 616–625.

    Google Scholar 

  • Bock, K. J. & Mann, H., 1971. Über anionenaktive Tenside im Küstengebiet der Nordsee. — Arch. Eisch. Wiss.22, 287–292.

    CAS  Google Scholar 

  • Bock, K. J. & Schöberl, P., 1977. Biologischer Abbau von Tensiden. In: Handbuch der Textilhilfsmittel. Hrsg. von A. Chwala & V. Anger. Verl. Chemie, Weinheim, 1045–1069.

    Google Scholar 

  • Bourdillon, A., 1954. Mise en évidence d'une substance favourisant la métamorphose des larves d'Alcyonium corralloides (von Koch). — C.r. hebd. Séanc. Acad. Sci., Paris239, 1434–1436.

    CAS  Google Scholar 

  • Cameron, R. A. & Hinegardner, R. T., 1974. Initiation of metamorphosis in laboratory cultured sea urchins. — Biol. Bull. mar. biol. Lab., Woods Hole.146, 335–342.

    CAS  Google Scholar 

  • Chia, F.-S. & Rice, M. E., 1978. Settlement and metamorphosis of marine invertebrate larvae. Elsevier, New York, 290 pp.

    Google Scholar 

  • Cloney, R. A., 1978. Ascidian metamorphosis, review and analysis. In: Settlement and metamorphosis of marine invertebrate larvae. Ed. by F.-S. Chia & M. E. Rice. Elsevier, New York, 255–282.

    Google Scholar 

  • Cole, H. A. & Knight-Jones, E. W., 1949. The settling behaviour of larvae of the European flat oysterOstrea edulis and its influence on methods of cultivation and spat collection. — Fishery Invest., Lond. (Ser. 2)17 (3), 1–39.

    Google Scholar 

  • Colman, J., 1933. The nature of intertidal zonation of plants and animals. — J. mar. biol. Ass. U.K.18, 435–476.

    Google Scholar 

  • Cori, C. J., 1939. Phoronidea. — Bronn's Kl. Ordn. Tierreichs4, Abt. 4, Buch 1, T. 1, 1–183.

    Google Scholar 

  • Crisp, D. J., 1953. Selection of site and position by some marine larvae. — Br. J. Anim. Behav.1, 80–81.

    Google Scholar 

  • Crisp, D. J., 1956. Surface chemistry, a factor in the settlement of marine invertebrate larvae. —Botanica Gothoburg.3, 51–65.

    Google Scholar 

  • Crisp, D. J., 1974. Factors influencing the settlement of marine invertebrate larvae. In: Chemoreception in marine organisms. Ed. by P. T. Grant & A. M. Mackie. Acad. Press, London, 177–265.

    Google Scholar 

  • Crisp, D. J. & Meadows, P. S., 1962. The chemical basis of gregariousness in cirripedes. — Proc. R. Soc. (B)156, 500–520.

    CAS  Google Scholar 

  • Crisp, D. J. & Meadows, P. S., 1963. Adsorbed layers: the stimulus to settlement in barnacles. — Proc. R. Soc. (B)158, 364–387.

    CAS  Google Scholar 

  • Crisp, D. J. & Ryland, J. S., 1960. Influence of filming surface texture on the settlement of marine organisms. — Nature, Lond.185, 119.

    Google Scholar 

  • Culliney, J. L., 1975. Comparative larval development of the shipwormsBankia gouldi andTeredo navalis. — Mar. Biol.29, 245–251.

    Article  Google Scholar 

  • Day, J. H. & Wilson, D. P., 1934. On the relation of the substratum to the metamorphosis ofScolecolepsis fuliginosa. — J. mar. biol. Ass. U.K.19, 655–662.

    Google Scholar 

  • Dietrich, G. & Kalle, K., 1965. Allgemeine Meereskunde. Bornträger, Berlin, 492 pp.

    Google Scholar 

  • Eiben, R., 1976. Einfluß von Benetzungsspannung und Ionen auf die Substratbesiedelung und das Einsetzen der Metamorphose bei Bryozoenlarven (Bowerbankia gracilis). — Mar. Biol.37, 249–254.

    Article  CAS  Google Scholar 

  • Eiben, R., Wieker, F. & Müller, W. A., 1976. Bakterien und Benetzungsspannung bestimmen das Festhalten und die Metamorphose mariner Substratbewohner. — Naturwissenschaften63, 45.

    Article  Google Scholar 

  • Goldberg, E. D., 1965. Minor elements in sea water. In: Chemical oceanography I. Ed. by J. P. Pieley & G. Skirrow. Acad. Press, London, 163–196.

    Google Scholar 

  • Grave, G. & Nicoll, P. A., 1939. Studies of larval life and metamorphosis inAscidia nigra and species ofPolyandrocarpa. — Publs Carnegie Instn517, 1–46.

    Google Scholar 

  • Gray, J. S., 1966. Attractive factor of intertidal sands toProtodrilus symbioticus. — J. mar. biol. Ass. U.K.46, 627–647.

    Google Scholar 

  • Gunkel, W., 1964. Die Verwendung des Ultra-turrax zur Aufteilung von Bakterienaggregaten in marinen Proben. — Helgoländer wiss. Meeresunters.11, 287–297.

    Google Scholar 

  • Gunkel, W., 1968. Die Fluktuation der Bakterien im jahreszeitlichen Verlauf in der Nordsee. —Veröff. Inst. Meeresforsch., Bremerhaven3, 121–124.

    Google Scholar 

  • Haas, W., Granzer, M. & Brockelman, C. R., 1990.Opisthorchis viverrini: finding and recognition of the first host by the cercariae. — Exp. Parasit.71, 422–431.

    CAS  PubMed  Google Scholar 

  • Hadfield, M. G., 1976. Molluscs associated with living tropical corals. — Micronesica12, 133–148.

    Google Scholar 

  • Hadfield, M. G. 1978. Metamorphosis in marine molluscan larvae: an analysis of stimulus and response. In: Settlement and metamorphosis of marine invertebrate larvae. Ed. by F.-S. Chia & M. E. Rice. Elsevier, New York, 165–176.

    Google Scholar 

  • Hadfield, M. G. & Karlson R. H., 1969. Externally induced metamorphosis in a marine gastropod. —Am. Zool.9, 1122.

    Google Scholar 

  • Hagmeier, E., 1978. Variations in phytoplankton near Helgoland. — Rapp. P.-v. Réun. Cons. int. Explor. Mer172, 261–363.

    Google Scholar 

  • Harington, C. R., 1921. A note on the physiology of the ship-worm (Teredo norvegica). — Biochem. J.15, 736–741.

    CAS  Google Scholar 

  • Harrigan, J. F., 1972. Behavior of the planula larva of the scleractinian coralPocillopora damicornis (L.). — Am. Zool.12, 723.

    Google Scholar 

  • Hasper, M., 1913. On a method of rearing larvae of Polyzoa. — J. mar. biol. Ass. U.K.9, 435–436.

    Google Scholar 

  • Hermans, C. O., 1978. Metamorphosis in the opheliid polychaeteArmandia brevis. In: Settlement and metamorphosis of marine invertebrate larvae. Ed. by F.-S. Chia & M. E. Rice. Elsevier, New York, 113–126.

    Google Scholar 

  • Herrmann, K., 1973. Dokumentation des Metamorphoseablaufs beiActinotrocha branchiata (Phoronida). — Helgoländer wiss. Meeresunters.25, 473–485.

    Article  Google Scholar 

  • Herrmann, K., 1975a. Einfluß von Bakterien auf die Metamorphoseauslösung und deren Verlauf beiActinotrocha branchiata (Phoronis mülleri). — Verh. dt. zool. Ges.1974, 112–115.

    Google Scholar 

  • Herrmann, K., 1975b.Phoronis mülleri (Tentaculata), Metamorphose derActinotrocha branchiata. —Publ. wiss. Film (Sekt. Biol.)8, 119–135.

    Google Scholar 

  • Herrmann, K., 1976. Untersuchungen über Morphologie, Physiologie und Ökologie der Metamorphose vonPhoronis mülleri. — Zool. Jb. (Anat. Ontogenie Tiere)95, 354–426.

    Google Scholar 

  • Herrmann, K., 1979. Larvalentwicklung und Metamorphose vonPhoronis psammophila (Tentaculata). — Helgoländer wiss. Meeresunters.32, 550–581.

    Article  Google Scholar 

  • Herrmann, K., 1981.Psammechinus miliaris: die Metamorphose aberranter Formen. — Publ. wiss. Film (Sekt. Biol.: Ser. 14)3, 1–22.

    Google Scholar 

  • Herrmann, K., 1983.Psammechinus miliaris: Metamorphose. — Publ. wiss. Film (Sekt. Biol.: Ser. 16)3, 1–19.

    Google Scholar 

  • Herrmann, K., 1986. Die Metamorphose vonPolygordius appendiculatus (Polychaeta, Archiannelida): Induktion und Ablauf. — Publ. wiss. Film (Sekt. Biol. Ser. 18)36, 1–15.

    Google Scholar 

  • Hickel, W. & Gunkel, W., 1968. Untersuchungen über die Häufigkeit der Bakterien in der obersten Sedimentschicht der Deutschen Bucht in Beziehung zu den Substrateigenschaften. — Helgoländer wiss. Meeresunters.18, 213–231.

    Article  Google Scholar 

  • Hofmann, D. K. & Brand, H., 1987. Induction of metamorphosis in the symbiotic scyphozoanCassiopea andromeda: role of marine bacteria and of biochemicals. — Symbiosis4, 99–116.

    Google Scholar 

  • Ikeda, I., 1901. Observations of the development, structure and metamorphosis of Actinotrocha. — J. Coll. Sci. imp. Univ. Tokyo13, 507–591.

    Google Scholar 

  • Jägersten, G., 1940. Die Abhängigkeit der Metamorphose vom Substrat des Biotops beiProtodrilus. — Ark. Zool.32 (17), 1–12.

    Google Scholar 

  • Kato, T., Kumarireng, A. S., Ichinose, J., Kitahara, Y., Kakinuma, Y., Nishihara, M. & Kato, M., 1975. Active components ofSargassum tortile effecting the settlement of swimming larvae ofCoryne uchidai. — Experientia 31, 433–434.

    Article  CAS  PubMed  Google Scholar 

  • Keck, R., Maurer, D., Kauer, J. C. & Sheppard, W. A., 1971. Chemical stimulants affecting larval settlement in the American oyster. — Proc. natn. Shellfish. Ass.60, 24–28.

    Google Scholar 

  • Knight-Jones, E. W., 1951. Gregariousness and some other aspects of the settling behaviour ofSpirorbis. — J. mar. biol. Ass. U.K.30, 201–222.

    Google Scholar 

  • Knight-Jones, E. W., 1953. Laboratory experiments on gregariousness during settling inBalanus balanoides and other barnacles. — J. exp. Biol.30, 584–598.

    CAS  Google Scholar 

  • Kriegstein, A. R., Catellucci, V. & Kandel, E. R., 1974. Metamorphosis ofAplysia california in laboratory culture. — Proc. natn. Acad. Sci. USA71, 3654–3658.

    CAS  Google Scholar 

  • Larman, V. N. & Gabbott, P. A., 1975. Settlement of cyprid larvae ofBalanus balanoides andElminius modestus induced by extracts of adult barnacles and other marine animals. — J. mar. biol. Ass. U.K.55, 183–190.

    Google Scholar 

  • Lynch, W. F., 1961. Extrinsic factors influencing metamorphosis in Bryozoan and Ascidian larvae. —Am. Zool.1, 59–66.

    Google Scholar 

  • Meadows, P. S. & Williams, G. B., 1963. Settlement ofSpirorbis borealis larvae on surface bearing films of micro-organisms. — Nature, Lond.198, 610–611.

    Google Scholar 

  • Moyse, J., 1971. Settlement and growth pattern of the parasitic barnaclePyrogma anglicum. In: Fourth European Marine Biology Symposium. Ed. by D. J. Crisp. Cambridge Univ. Press, Cambridge, 125–141.

    Google Scholar 

  • Müller, W. A., 1969. Auslösung der Metamorphose durch Bakterien bei den Larven vonHydractinia echinata. — Zool. Jb. (Anat. Ontogenie Tiere)86, 84–95.

    Google Scholar 

  • Müller, W. A., 1973. Metamorphose-Induktion bei Planula-Larven: I. Der bakterielle Induktor. —Wilhelm Roux Arch. EntwMech. Org.173, 107–121.

    Google Scholar 

  • Müller, W. A. & Buchal G., 1973. Metamorphose-Induktion bei Planula-Larven: II. Induktion durch monovalente Kationen. — Wilhelm Roux Arch. EntwMech. Org.173, 122–135.

    Google Scholar 

  • Neu, W., 1933. Der Einfluß des Farbtons der Unterlage auf die Besiedelung mitBalanus undSpirorbis. — Int. Revue ges. Hydrobiol. Hydrogr.28, 228–246.

    Google Scholar 

  • Neumann, R., 1979. Bacterial induction of settlement and metamorphosis in the planula larvae ofCassiopea andromeda. — Mar. Ecol. Prog. Ser.1, 21–28.

    Google Scholar 

  • Newman, W. A. & Ross, A., 1976. Revision of the balanomorph barnacles inducing a catalog of the species. — Mem. S. Diego Soc. nat. Hist.9, 1–108.

    Google Scholar 

  • Nishihira, M., 1967. Observations on the selection of algal substrata by hydrozoan larvaeSertularella miurenis in nature. — Bull. biol. Stn. Asamushi13, 35–48.

    Google Scholar 

  • Nishihira, M., 1968. Experiments on the algal selection by the larvae ofCoryne urchidai Stechow (Hydrozoa). — Bull. biol. Stn. Asamushi13, 83–89.

    Google Scholar 

  • Nyholm, K. G., 1950. Contributions to the life-history of the Ampharetid,Melinna cristata. — Zool. Bidr. Upps.29, 79–81.

    Google Scholar 

  • Perron, F. E. & Turner, R. D., 1977. Development, metamorphosis and natural history of the nudibranchDoridella obscura Verrill (Corambidae, Opisthobranchia). — J. exp. mar. Biol. Ecol.27, 171–185.

    Article  Google Scholar 

  • Prefinch, K. A. & Downing, F. S., 1949. Notes on the general biology ofTubularia larynx. — J. mar. biol. Ass. U.K.28, 21–23.

    Google Scholar 

  • Rice, M. E., 1978. Morphological and behavioral changes at metamorphosis in the Sipunculida. In: Settlement and metamorphosis of marine invertebrate larvae. Ed. by F.-S. Chia & M. E. Rice. Elsevier, New York, 83–102.

    Google Scholar 

  • Rieper, M., 1976. Investigations on the relationship between algal blooms and bacterial populations in the Schlei Fjord (Western Baltic Sea). — Helgoländer wiss. Meeresunters.28, 1–18.

    Article  Google Scholar 

  • Rockstroh, T., 1967. Über die Wirkung der Detergentien auf die Morphologie einer Ciliatenzelle. —Acta biol. med. germ.19, 161–184.

    CAS  PubMed  Google Scholar 

  • Runnström, J. & Runnström, S., 1919. Über die Entwicklung vonCucumaria frondosa Gunerus undPsolus phantapus Strussenf. — Bergens Mus. Årb. (Naturv. R.)5, 1–99.

    Google Scholar 

  • Scheer, B. T., 1945. The development of marine fouling communities. — Biol. Bull. mar. biol. Lab., Woods Hole89, 103–121.

    Google Scholar 

  • Scheltema, R. S., 1961. Metamorphosis of the veliger-larvae ofNassarius obsoletus (Gastropoda) in response to bottom sediment. — Biol. Bull. mar. biol. Lab., Woods Hole120, 92–109.

    Google Scholar 

  • Schneider, A., 1862. Über die Metamorphose derActinotrocha branchiata. — Arch. Anat. Physiol.1862, 47–65.

    Google Scholar 

  • Schwoerer-Böhning, B., Kroiher, M. & Müller, W. A., 1990. Signal transmission and covert prepattern in the metamorphosis ofHydractinia echinata (Hydrozoa). — Wilhelm Roux Arch. dev. Biol.198, 245–251.

    Google Scholar 

  • Siewing, R., 1969. Lehrbuch der vergleichenden Entwicklungsgeschichte der Tiere. Parey, Hamburg, 531 pp.

    Google Scholar 

  • Siewing, R., 1974. Morphologische Untersuchungen zum Archicoelomatenproblem: 2. Die Körpergliederung beiPhoronis mülleri. — Zool. Jb. (Anat. Ontogenie Tiere)92, 275–318.

    Google Scholar 

  • Silén, L., 1954. Developmental biology of Phoronidea of the Gullmar Fjord (west coast of Sweden). —Acta zool., Stockh.35, 215–257.

    Google Scholar 

  • Spindler, K. D. & Müller, W. A., 1972. Induction of metamorphosis by bacteria and by lithium-pulse in the larvae ofHydractinia echinata (Hydrozoa). — Wilhelm Roux Arch. EntwMech. Org.169, 271–280.

    Article  Google Scholar 

  • Swedmark, M., Braaten, B., Emanuelsson, E. & Granmo, A., 1971. Biological effects of surface active agents on marine animals. — Mar. Biol.9, 183–201.

    Article  CAS  Google Scholar 

  • Swennen, C., 1961. Data on distribution, reproduction and ecology of the nudibranchiate molluscs occurring in the Netherlands. — Neth. J. Sea Res.1, 191–240.

    Google Scholar 

  • Switzer-Dunlap, M., 1978. Larval biology and metamorphosis of aplysiid gastropods. In: Settlement and metamorphosis of marine invertebrate larvae. Ed. by F.-S. Chia & M. E. Rice. Elsevier, New York, 197–206.

    Google Scholar 

  • Switzer-Dunlap, M. & Hadfield, M. G., 1977. Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropoda, Opisthobranchia) in laboratory culture. — J. exp. mar. Biol. Ecol.29, 245–261.

    Article  Google Scholar 

  • Thompson, T. E., 1962. Studies on the ontogeny ofTritonia hombergi Curvier (Opisthobranchia). —Phil. Trans. R. Soc. (Ser. B)245, 171–218.

    Google Scholar 

  • Wieker, F., 1975. Bildung und Metamorphose der Schwimmknospen vonCassiopea xamachana. —Dipl.-Arb., Univ. Braunschweig, 119 pp.

  • Wilson, D. P., 1932. On the mitraria larva ofOwenia fusiformis. — Phil. Trans. R. Soc. (Ser. B)221, 231–334.

    Google Scholar 

  • Wilson, D. P., 1937. The influence of the substratum on the metamorphosis ofNotomastus larvae. — J. mar. biol. Ass. U.K.22, 227–243.

    Google Scholar 

  • Wilson, D. P., 1948. The relation of substratum to the metamorphosis ofOphelia larvae. — J. mar. biol. Ass. U.K.27, 723–760.

    Google Scholar 

  • Wilson, D. P., 1952. The influence of the nature of the substratum on the metamorphosis of the larvae of marine animals, especially the larvae ofOphelia bicornis. — Annls Inst. ocanogr.27, 49–156.

    Google Scholar 

  • Wilson, D. P., 1955. The role of micro-organisms in the settlement ofOphelia bicornis Savigny. — J. mar. biol. Ass. U.K.34, 531–543.

    Google Scholar 

  • Wilson, D. P., 1968. The settlement behaviour of the larvae ofSabellaria alveolata. — J. mar. biol. Ass. U.K.,48, 387–435.

    Google Scholar 

  • Wilson, D. P., 1970. The larvae ofSabellaria spinulosa and their settlement behaviour. — J. mar. biol. Ass. U.K.50, 33–52.

    Google Scholar 

  • Yonge, C. M., 1937. The biology ofAporrhais pes-pelicani andA. serresiana. — J. mar. biol. Ass. U.K.21, 687–703.

    Google Scholar 

  • Zinkin, L. N., 1938. Stimulation of metamorphosis in ascidian larvae. — Dokl. Akad. Nauk SSSR for. Lang. Edn18 (3), 213–216.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Herrmann, K. Induction and regulation of metamorphosis in planktonic larvae:Phoronis mülleri (Tentaculata) as archetype. Helgolander Meeresunters 49, 255–281 (1995). https://doi.org/10.1007/BF02368355

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02368355

Keywords