Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-26T19:53:38.970Z Has data issue: false hasContentIssue false
  • English
  • Français

Larval metamorphosis of the opisthobranch mollusc Adalaria proxima (Gastropoda: Nudibranchia): the effects of choline and elevated potassium ion concentration

Published online by Cambridge University Press:  11 May 2009

Christopher D. Todd ,
Matthew G. Bentley  and
Jonathan N. Havenhand
Christopher D. Todd
Affiliation:
Gatty Marine Laboratory, Department of Biology & Pre-Clinical Medicine, University of St Andrews, Fife, KYI 6 8LB
Matthew G. Bentley
Affiliation:
Gatty Marine Laboratory, Department of Biology & Pre-Clinical Medicine, University of St Andrews, Fife, KYI 6 8LB
Jonathan N. Havenhand
Affiliation:
Gatty Marine Laboratory, Department of Biology & Pre-Clinical Medicine, University of St Andrews, Fife, KYI 6 8LB
Get access Rights & Permissions [Opens in a new window]

Extract

Veliger larvae of the nudibranch mollusc Adalaria proxima are triggered to metamorphose to the benthic form by the adult prey bryozoan, Electro pilosa. Ion substitution and supplementation experiments with artificial sea water (ASW) have, however, shown that metamorphosis can be induced by elevation of the potassium ion concentration alone. Approximately 19 mM K+ASW (10 mM ‘excess’) was found to elicit maximal metamorphic responses: 29 and 39 mM K+ASW had no inductive effect. Choline chloride was also found to induce metamorphosis in a dose-dependent manner, with lO M ineffective, 10 M approximately threshold, and 5×10 M to 10 M optimal. Concentrations of choline >10 M were sub-lethally toxic. That the absence of larval metamorphosis on exposure to 29 and 39 mM K ASW was due to inhibition is inferred from interaction experiments with choline: at these concentrations of K, metamorphosis in response to choline could be abolished. Timed-exposure experiments indicated that artificial induction elicited by elevated K and choline involve either separate mechanisms, or different parts of the same pathway. Thus, whilst larvae required to be continuously exposed to 19 mM K ASW in order to complete metamorphosis, those exposed to 10 M choline would subsequently complete development in normal ASW following only 1–2 h exposure to the inducer. Preliminary experiments failed to specify further the nature of the natural inducer, beyond the confirmation that live intact colonies of the bryozoan Electro pilosa will trigger larvae to metamorphose.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 71 , Issue 1 , February 1991 , pp. 53 - 72
Copyright
Copyright © Marine Biological Association of the United Kingdom 1991

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

ArkettS.A., S.A.,ChiaF.-S., F.-S.,Goldberg, J.I. & KossR., R., 1989. Identified settlement receptor cells in a nudibranch veliger respond to specific cue. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 176, 155–160.CrossRefGoogle Scholar
Baloun, A.J. & MorseD.E., D.E., 1984. Ionic control of settlement and metamorphosis in larval Haliotis rufescens (Gastropoda). Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 167, 124–138.CrossRefGoogle Scholar
Baxter, G. & MorseD.E., D.E., 1987. G protein and diacylglycerol regulate metamorphosis of planktonic molluscan larvae. Proceedings of the National Academy of Sciences of the United States of America, 84,1867–1870.CrossRefGoogle ScholarPubMed
BoucherL.M., L.M., 1986. Vestigial larval shells in the planktonic veligers of two gymnodorid nudibranchs. Journal of Molluscan Studies, 52, 30–34.CrossRefGoogle Scholar
Cameron, R.A. & HinegarderR.T., R.T., 1974. Initiation of metamorphosis in laboratory cultured sea urchins. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 146, 335–342.CrossRefGoogle ScholarPubMed
CargoD.G., D.G., 1975. Comments on the laboratory culture of Scyphozoa. In Culture of Marine Invertebrate Animals (ed. Smith, W.L. and Chanley, M.H.), pp. 145–154. New York: Plenum Press.CrossRefGoogle Scholar
Chia, F.-S. & KossR., R., 1988. Induction of settlement and metamorphosis of the veliger larva of the nudibranch Onchidoris bilamellata. International Journal of Invertebrate Reproduction and Development, 14,53–70.CrossRefGoogle Scholar
CochardJ.C., J.C.,CherolotL., L.,Yvin, J.C. & Chevolot-MagueurA.M., A.M., 1989. Induction de la métamorphose de la coquille Saint Jacques Pecten maximus L. par des dérivés de la tyrosine extraits de l'algue Delesseria sanguinea Lamoroux ou synthétiques. Haliotis, 19, 259–274.Google Scholar
CoonS.L., S.L., & BonarD.B., D.B., 1986. Norepinephrine and dopamine content of larvae and spat of the Pacific oyster, Crassostrea gigas. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 171, 632–639.CrossRefGoogle ScholarPubMed
CoonS.L., S.L., & BonarD.B., D.B., 1987. Pharmacological evidence that alphaj-adrenoceptors mediate metamorphosis of the Pacific oyster, Crassostrea gigas. Neuroscience, 23,1169–1174.CrossRefGoogle ScholarPubMed
CoonS.L., S.L.,BonarD.B., D.B., & WeinerR.M., R.M., 1985. Induction of settlement and metamorphosis of the Pacific oyster, Crassostrea gigas, by L-DOPA and catecholamines. Journal of Experimental Marine Biology and Ecology, 94,211–221.CrossRefGoogle Scholar
CoonS.L., S.L.,Bonar, D.B. & WeinerR.M., R.M., 1986. Chemical production of cultchless oyster spat using epinephrine and norepinephrine. Aquaculture, 58, 255–262.CrossRefGoogle Scholar
CrispD.J., D.J., 1974. Factors influencing the settlement of marine invertebrate larvae. In Chemoreception in Marine Organisms (ed. Grant, P.T. and Mackie, A.M.) pp. 177–265. New York: Academic Press.Google Scholar
Eyster, L.S. & PechenikJ.A., J.A., 1987. Attachment of Mytilus edulis (L.) larvae on algal and byssal filaments is enhanced by water agitation. Journal of Experimental Marine Biology and Ecology, 114, 99–110.CrossRefGoogle Scholar
Eyster, L.S. & PechenikJ.A., J.A., 1988. Comparison of growth, respiration and feeding of juvenile Crepidula fornicata (L.) following natural or KCl-triggered metamorphosis. Journal of Experi-mental Marine Biology and Ecology, 118, 269–279.CrossRefGoogle Scholar
GuillardR.R.L., R.R.L., 1975. Culture of phytoplankton for feeding marine invertebrates. In Culture of Marine Invertebrate Animals (ed. Smith, W.L. and Chanley, M.H.), pp. 29–60. New York: Plenum Press.CrossRefGoogle Scholar
HadfieldM.G., M.G., 1977. Chemical interactions in larval settling of a marine gastropod. In Marine Natural Products Chemistry, (ed. Faulkner, D.J. and Fenical, W.H.) pp. 403–413. New York: Plenum Press.CrossRefGoogle Scholar
HadfieldM.G., M.G., 1978. Metamorphosis in marine molluscan larvae: an analysis of stimulus and response. In Settlement and Metamorphosis of Marine Invertebrate Larvae, (ed. Chia, F.-S. and Rice, M.E.) pp. 165–175. New York: Elsevier.Google Scholar
HadfieldM.G., M.G., 1984. Settlement requirements of molluscan larvae: new data on chemical and genetic roles. Aquaculture, 39, 283–298.CrossRefGoogle Scholar
Hadfield, M.G. & PenningtonJ.T., J.T., 1990. Nature of the metamorphic signal and its internal transduction in larvae of the nudibranch Phestilla sibogae. Bulletin of Marine Science, 46, 455–464.Google Scholar
Hadfield, M.G. & ScheuerD., D., 1985. Evidence for a soluble metamorphic inducer in Phestilla: ecological, chemical and biological data. Bulletin of Marine Science, 37, 556–566.Google Scholar
HarrisL.G., L.G., 1973. Nudibranch associations. In Current Topics in Comparative Pathobiology, (ed. Cheng, T.C.) pp. 77–90. London: University Press.Google Scholar
Hirata, K.Y. & HadfieldM.G., M.G., 1986. The role of choline in metamorphic induction of Phestilla (Gastropoda: Nudibranchia). Comparative Biochemistry and Physiology, 84C, 15–21.Google Scholar
Hodgkin, A.L. & KatzB., B., 1949. The effect of sodium ions on the electrical activity of the giant axon of the squid. Journal of Physiology, 108, 37–77.CrossRefGoogle ScholarPubMed
HubbardE.J.A., E.J.A., 1988. Larval growth and the induction of metamorphosis of a tropical sponge-eating nudibranch. Journal of Molluscan Studies, 54,259–269.CrossRefGoogle Scholar
KempfS.C., S.C., 1981. Long-lived larvae of the gastropod Aplysia Juliana: do they disperse and metamorphose or just slowly fade away? Marine Ecology Progress Series, 6, 61–65.Google Scholar
Kempf, S.C. & ToddCD., CD., 1989. Feeding potential in the lecithotrophic larvae of Adalaria proximo and Tritonia hombergi: an evolutionary perspective. Journal of the Marine Biological Association of the United Kingdom, 69, 659–682.CrossRefGoogle Scholar
KesterD.R., D.R.,DuedallI.W., I.W.,Connors, D.N. & PytokowiczR.M., R.M., 1967. Preparation of artificial sea water. Limnology and Oceanography, 12, 176–179.CrossRefGoogle Scholar
Lyman, J. & FlemingR.H., R.H., 1940. Composition of sea water. Journal of Marine Research, 3,134–146.Google Scholar
Maki, J.S. & MitchellR., R., 1985. Involvement of lectins in the settlement and metamorphosis of marine invertebrate larvae. Bulletin of Marine Science, 37, 675–683.Google Scholar
MorseD.E., D.E., 1985. Neurotransmitter-mimetic inducers of larval settlement and metamorphosis. Bulletin of Marine Science, 37, 697–706.Google Scholar
MorseD.E., D.E.,HookerM., M.,DuncanH., H., & JensenL., L., 1979. γ-Aminobutyric acid, neurotransmitter, induces planktonic abalone larvae to settle and begin metamorphosis. Science, New York, 204, 407–410.CrossRefGoogle ScholarPubMed
MorseD.E., D.E.,TegnerM., M.,DuncanH., H.,HookerN., N.,Trevelyan, G. & CameronA., A., 1980. Induction of settling and metamorphosis of planktonic molluscan larvae. III. Signaling by metabolites of intact algae is dependent on contact. In Chemical Signaling in Vertebrate and Aquatic Animals (ed. Müller-Schwarze, D. and Silverstein, R.M.), pp. 67–86. New York: Plenum Press.Google Scholar
MüllerW.A., W.A., 1973. Metamorphose-induktion bei Planulalarven. I. Der Bakterielle Induktor. Wilhelm Roux' Archives for Developmental Biology, 173,107–121.CrossRefGoogle Scholar
Müller, W.A. & BuchalG.I., G.I., 1973. Metamorphose-induktion bei Planulalarven. II. Die Bedentung des Gibbs-Donnan-Verhältnisses und der Na+/K+ ATP-ase. Wilhelm Roux' Archives for Developmental Biology, 173, 122–135.CrossRefGoogle Scholar
Nell, J.A. & HollidayJ.E., J.E., 1986. Effects of potassium and copper on the settling rate of Sydney rock oyster (Saccostrea commercialis) larvae. Aquaculture, 58,263–267.CrossRefGoogle Scholar
NicolJ.A.C., J.A.C., 1960. The Biology of Marine Animals. London: Pitman.CrossRefGoogle Scholar
ParsonsT.R., T.R.,Takahashi, M. & HargraveB., B., 1984. Biological Oceanographic Processes. Oxford: Pergamon Press.Google Scholar
PawlikJ.R., J.R., 1990. Natural and artificial induction of metamorphosis of Phragmatopoma lapidosa californica (Polychaeta: Sabellariidae), with a critical look at the effects of bioactive compounds on marine invertebrate larvae. Bulletin of Marine Science, 46, 512–536.Google Scholar
Pechenik, J.A. & HeymanW.D., W.D., 1987. Using KC1 to determine size at competence for the larvae of the marine gastropod Crepidula fornicata (L.). Journal of Experimental Marine Biology and Ecology, 112, 27–38.CrossRefGoogle Scholar
RittschofD., D.,MakiJ., J.,Mitchell, R. & CostlowJ.D., J.D., 1986. Ion and neuropharmacological ses of barnacle settlement. Netherlands journal of Sea Research, 20, 269–275.CrossRefGoogle Scholar
ThompsonT.E., T.E., 1958. The natural history, embryology, larval biology and post-larval development of Adalaria proximo (Alder & Hancock) (Gastropoda, Opisthobranchia). Philosophical Transactions of the Royal Society(B), 242, 1–58.Google Scholar
ThompsonT.E., T.E., 1958. Studies on the ontogeny of Tritonia hombergi Cuvier (Gastropoda, Opisthobranchia). Philosophical Transactions of the Royal Society (B), 245, 171–218.Google Scholar
ToddC.D., C.D., 1981. The ecology of nudibranch molluscs. Oceanography and Marine Biology, an Annual Review, 19,141–234.Google Scholar
Todd, C.D. & HavenhandJ.N., J.N., 1985. Preliminary observations on the embryonic and larval development of three dorid nudibranchs. Journal of Molluscan Studies, 52, 226–228.Google Scholar
ToddC.D., C.D.,Havenhand, J.N. & ThorpeJ.P., J.P., 1988. Genetic differentiation, pelagic larval transport and gene flow between local populations of the intertidal marine mollusc Adalaria proximo (Alder & Hancock). Functional Ecology, 2,441–451.CrossRefGoogle Scholar
Todd, C.D. & TurnerS.J., S.J., 1986. Ecology of intertidal and sublittoral cryptic epifaunal assemblages. I. Experimental rationale and the analysis of larval settlement. Journal of Experimental Marine Biology and Ecology, 99, 199–231.CrossRefGoogle Scholar
Trapido-Rosenthal, H.G. & MorseD.E., D.E., 1985. L-α,ωdiamino acids facilitate GABA induction of larval metamorphosis in a gastropod mollusc (Haliotis rufescens). Journal of Comparative Physiology, 155(B), 403–414.CrossRefGoogle Scholar
Vinson, G.P. & KenyonC.J., C.J., 1978. Steroidogenesis in the zones of the mammalian adrenal cortex. In General, Comparative and Clinical Endocrinology of the Adrenal Cortex (ed. Chester-Jones, I. and Henderson, I.W.), pp. 201–264. London: Academic Press.CrossRefGoogle Scholar
YoolA.J., A.J.,GrauS.M., S.M.,HadfieldM.G., M.G.,JensenR.A., R.A.,Maskell, D.A. & MorseD.E., D.E., 1986. Excess potassium induces larval metamorphosis in four marine invertebrate species. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 170, 255–266.CrossRefGoogle Scholar