Abstract
Marine invertebrates settle, attach, and/or metamorphose in response to signals from several sources, including seaweeds. In response to the aquaculture challenge of producing constant numbers of juveniles from cultured species, natural inducers have been screened for their ability to improve those processes. However, few chemical inducers of attachment of invertebrates have been identified, and even less of these were secondary metabolites. The goal of this work was to isolate the natural products responsible for induction activity using bioassay-guided fractionation of the organic extract of the brown seaweed Stypopodium zonale and the attachment of juveniles of the common brown mussel, Perna perna, as a model. The meroditerpene epitaondiol, identified by comparison of spectral data with the literature, promoted as much as 4.7 times more mussel attachment compared to controls at the natural concentration found in this alga (0.041% of the crude extract or 0.012% of algal dry weight). This is the first report showing that a seaweed produces terpenoid compounds as cues for invertebrate attachment, and future studies evaluating this action on settlement of mussels in the field are expected to improve aquaculture technology by increasing mussel spat production.
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Abessa DMS, Zaroni LP, Souza ECPM, Gasparro MR, Pereira CDS, Rachid BRF, Depledge M, King RS (2005) Pysiological and cellular responses in two populations of the mussel Perna perna collected at different sites from the coast of São Paulo, Brazil. Braz Arch Biol Technol 48, 217–225
Alfaro AC, Jeffs AG (2003) Variability in mussel settlement on suspended ropes placed in Ahipara Bay, Northland, New Zealand. Aqua Res 216, 115–126
Alfaro AC, Jeffs AG, Creese RG (2004) Bottom-drifting algal/mussel spat associations along a sandy coastal region in northern New Zealand. Aquaculture 241, 269–290
Baker P, Mann R (1997) The postlarval phase of bivalve molluscs: a review of functional ecology and new records of postlarval drifting of Chesapeake Bay bivalves. Bull Mar Sci 61, 409–430
Brumbaugh RD, McConaugha JR (1995) Time to metamorphosis of blue crab Callinectes sapidus megalopae: effects of benthic macroalgae. Mar Ecol Prog Ser 129, 113–118
Buchanan S, Babcock R (1997) Primary and secondary settlement by the greenshell mussel Perna canaliculus. J Shellfish Res 16, 71–76
Coll JC, Bowden BF (1986) The application of vacuum liquid chromatography to the separation of terpene mixtures. J Nat Prod 49, 934–936
Da Gama BAP, Pereira RC, Carvalho AGV, Coutinho R, Yoneshigue-Valentin Y (2002) The effects of seaweed secondary metabolites on biofouling. Biofouling 18, 13–20
Da Gama BAP, Pereira RC, Soares AR, Teixeira VL, Yoneshigue-Valentin Y (2003) Is the mussel test a good indicator of antifouling activity? A comparison between laboratory and field assays. Biofouling 19, 161–169
Da Silva PM, Magalhaes ARM, Barracco MA (2002) Effects of Bucephalus sp (Trematoda: Bucephalidae) on Perna perna mussels from a culture station in ratones Grande Island, Brazil. J Invert Pathol 79, 154–162
Daume S, Brand-Gardner S, Woelkerling WJ (1999) Settlement of abalone larvae (Haliotis laevigata Donovan) in response to non-geniculate coralline red algae (Corallinales, Rodhophyta). J Exp Mar Biol Ecol 234, 125–143
Davis AR, Moreno CA (1995) Selection of substrata by juvenile Choromytilus chorus (Mytilidae): are chemical cues important? J Exp Mar Biol Ecol 191, 167–180
Decho AW, Browne KA, Zimmer-Faust RK (1998) Chemical cues: Why basic peptides are signal molecules in marine environments. Limnol Oceanogr 43, 1410–1417
Dobretsov S, Qian P-Y (2003) Pharmacological induction of larval settlement and metamorphosis in the blue mussel Mytilus edulis L. Biofouling 19, 57–63
Dobretsov S, Qian P-Y (2004) The role of epibiotic bacteria from the surface of the soft coral Dendronephthya sp in the inhibition of larval settlement. J Exp Mar Biol Ecol 299, 35–50
Doroudi MS, Southgate PC (2002) The effect of chemical cues on settlement behavior of blacklip pearl oyster (Pinctada margaritifera) larvae. Aquaculture 209, 117–124
Eyster LS, Pechenik JA (1988) Attachment of Mytilus edulis L larvae on algal and byssal filaments is enhanced by water agitation. J Exp Mar Biol Ecol 114, 99–110
Fleck J, Fitt WK (1999) Degrading mangrove leaves of Rhizophora mangle Linne provide a natural cue for settlement and metamorphosis of the upside down jellyfish Cassiopea xamachana Bigelow. J Exp Mar Biol Ecol 234, 83–94
Forward RB Jr, DeVries MC, Rittschof D, Frankel DAZ, Bischoff JP, Fisher CM, Welch JM (1996) Effects of environmental cues on metamorphosis of the blue crab Callinectes sapidus. Mar Ecol Prog Ser 131, 165–177
Fusetani N (2004) Biofouling and antifouling. Nat Prod Rep 21, 94–104
Gallardo WG, Buen SMA (2003) Evaluation of mucus, Navicula, and mixed diatoms as larval settlement inducers for the tropical abalone Haliotis asinine. Aquaculture 221, 357–364
Gerwick WH, Fenical W (1981) Ichthyotoxic and cytotoxic metabolites of the tropical brown alga Stypopodium zonale (Lamouroux) Papenfuss. J Org Chem 46, 22–27
Gerwick WH, Fenical W, Norris JN (1985) Chemical variation in the tropical seaweed Stypopodium zonale (Dictyotaceae). Phytochemistry 24, 1279–1283
Gil B, Ferrandiz M, Sanz M, Terrencio M, Ubeda A, Rovirosa J, San-Martín A, Alcaraz M, Paya M (1995) Inhibition of inflammatory responses by epitaondiol and other marine metabolites. Life Sci 57, 25–30
Hadfield MG, Paul VJ (2001) Natural chemical cues for settlement and metamorphosis of marine invertebrate larvae. In: Marine Chemical Ecology, McClintock JB, Baker BJ eds. (Boca Raton, FL: CRC Press), pp 431–462
Hardege JD, Bentley MG, Snape L (1998) Sediment selection by juvenile Arenicola marina. Mar Ecol Prog Ser 166, 187–195
Hoagland P, Kite-Powell HL, Jin D (2003) Business Planning Handbook for the Ocean Aquaculture of Blue Mussels (Woods Hole, MA: Woods Hole Oceanographic Institution), pp 1–31
Kato T, Kumanireng AS, Ichinose I, Kitahara Y, Kakinuma Y, Nishihira M, Kato M (1975) Active components of Sargassum tortile affecting the settlement of swimming larvae of Coryne uchidai. Experientia 31, 433–434
Krug PJ, Manzi AE (1999) Waterborne and surface-associated carbohydrates as settlement cues for larvae of the specialist marine herbivore Alderia modesta. Biol Bull 197, 94–103
Lane DJW, Beaumont AR, Hunter JR (1985) Byssus drifting and the drifting threads of the young post-larval mussel Mytilus edulis. Mar Biol 84, 301–308
Lau SC, Qian P-Y (2001) Larval settlement in the serpulid polychaete Hydroides elegans in response to bacterial films: an investigation of the nature of putative larval settlement cue. Mar Biol 138, 321–328
Leitz T, Wagner T (1993) The marine bacterium Alteromonas espejiana induces metamorphosis of the hydroid Hydractinia echinate. Mar Biol 115, 173–178
Marenzi AWC, Branco JO (2005) O mexilhão Perna perna (Linnaeus) (Bivalvia, Mytilidae) em cultivo na Armação do Itapocoroy, Santa Catarina, Brazil. Rev Bras Zool 22, 394–399
McGee BL, Targett NM (1989) Larval habitat selection in Crepidula (L) and its effect on adult distribution patterns. J Exp Mar Biol Ecol 131, 195–214
Morse ANC (1990) Recent progress in larval settlement and metamorphosis: closing the gaps between molecular biology and ecology. Bull Mar Sci 46, 465–483
Okamoto K, Watanable A, Sakata K, Watanabe N (1998) Chemical signals involved in larval metamorphosis in Hydroides ezoensis (Serpulidae; Polychaeta). Part I: Induction of larval metamorphosis by extract of adult tube clumps. J Mar Biotechnol 6, 7–10
Paul VJ, Puglisi PM, Ritson-Williams R (2006) Marine chemical ecology. Nat Prod Rep 23, 153–180
Pawlik JR, Faulkner DJ (1986) Specific free fatty acids induce larval settlement and metamorphosis of the reef-building tube worm Phragmatopoma californica (Fewkes). J Exp Mar Biol Ecol 102, 301–310
Pearce CM, Scheibling RE (1990) Induction of metamorphosis of larvae of the green sea-urchin Strongylocentrotus droebachiensis, by coralline red algae. Biol Bull 179, 304–311
Pereira RC, Soares AR, Teixeira VL, Villaça R¸ da Gama BAP (2004) Variation in chemical defenses against herbivory in southwestern Atlantic Stypopodium zonale (Phaeophyta). Bot Mar 47, 202–208
Petersen JH (1984) Larval settlement behavior in competing species-Mytilus californianus Conrad and Mytilus edulis L. J Exp Mar Biol Ecol 82, 147–159
Roczanski M, Costa SW, Boll MG, Oliveira Neto FM (2000) A evolução da aqüicultura no estado de Santa Catarina-Brasil. In Anais do Aqüicultura Brasil 2000: Simpósio Brasileiro de Aquicultura, Florianópolis, Brasil 11, 1–9
Rovirosa J, San-Matín A (1997) Antimicrobial activity of the brown alga Stypopodium flabelliforme constituents. Fitoterapia 68, 473–475
Rovirosa J, Sepulveda M, Quezada E, San-Martín A (1992) Isoepitaondiol, a diterpenoid of Stypopodium flabelliforme and the insecticidal activity of stypotriol, epitaondiol and derivatives. Phytochemistry 31, 2679–2681
Sánchez-Ferrando F, San-Martín A (1995) Epitaondiol: the first polycyclic meroditerpenoid containing two fused six-membered rings forced into the twist-boat conformation. J Org Chem 60, 1475–1478
Slattery M (1992) Larval settlement and juvenile survival in the red abalone (Haliotis rufescens): an examination of inductive cues and substrate selection. Aquaculture 102, 143–153
Smaal AC (2002) European mussel cultivation along the Atlantic coast: production status, problems and perspectives. Hydrobiologia 484, 89–98
Steinberg PD, De Nys R, Kjelleberg S (2001) Chemical mediation of surface colonization In: Marine Chemical Ecology, McClintock JB, Baker BJ eds. (Boca Raton, FL: CRC Press), pp 355–387
Wessels M, König GM, Wright AD (1999) A new tyrosine kinase inhibitor from the marine brown macroalga Stypopodium zonale. J Nat Prod 62, 927–930
Wieczorek SK, Todd CD (1997) Inhibition and facilitation of bryozoan and ascidian settlement by natural multi-species biofilms: effects of film age and the roles of active and passive larval attachment. Mar Biol 128, 463–473
Wright JR, Boxshall AJ (1999) The influence of small-scale flow and chemical cues on the settlement of two congeneric barnacle species. Mar Ecol Prog Ser 183, 179–187
Young CM, Braithwaite LF (1980) Orientation and current-induced flow in the stalked ascidian Styela montereyensis. Biol Bull 159, 428–440
Yvin JC, Chevolot L, Chevolotmagueur AM, Cochard JC (1985) 1st isolation of jacaranone from an alga, Delesseria sanguinea-a metamorphosis inducer of pecten larvae.J Nat Prod 48, 814–816
Zhao B, Zhang S, Qian P-Y (2003) Larval settlement of the silver- or goldlip pearl oyster Pinctada maxima (Jameson) in response to natural biofilms and chemical cues. Aquaculture 220, 883–901
Acknowledgments
The authors thank CNPq and FAPERJ for financial support. B.A.P.G., V.L.T., and R.C.P. gratefully acknowledge CNPq (Brazilian National Research Council) for providing their Research Productivity fellowships. A.R.S. thanks CAPES and FAPERJ for PhD scholarships. Comments by five reviewers and N. Fusetani were invaluable in improving the manuscripts and are gratefully acknowledged.
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Soares, A.R., da Gama, B.A.P., da Cunha, A.P. et al. Induction of Attachment of the Mussel Perna perna by Natural Products from the Brown Seaweed Stypopodium zonale . Mar Biotechnol 10, 158–165 (2008). https://doi.org/10.1007/s10126-007-9048-7
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DOI: https://doi.org/10.1007/s10126-007-9048-7