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Chemical Ecology of Marine Angiosperms: Opportunities at the Interface of Marine and Terrestrial Systems

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Abstract

This review examines the state of the field for chemically mediated interactions involving marine angiosperms (seagrasses, mangroves, and salt marsh angiosperms). Small-scale interactions among these plants and their herbivores, pathogens, fouling organisms, and competitors are explored, as are community-level effects of plant secondary metabolites. At larger spatial scales, secondary metabolites from marine angiosperms function as reliable cues for larval settlement, molting, or habitat selection by fish and invertebrates, and can influence community structure and ecosystem function. Several recent studies illustrate the importance of chemical defenses from these plants that deter feeding by herbivores and infection by pathogens, but the extent to which allelopathic compounds kill or inhibit the growth of competitors is less clear. While some phenolic compounds such as ferulic acid and caffeic acid act as critical defenses against herbivores and pathogens, we find that a high total concentration of phenolic compounds within bulk plant tissues is not a strong predictor of defense. Residual chemical defenses prevent shredding or degradation of plant detritus by detritivores and microbes, delaying the time before plant matter can enter the microbial loop. Mangroves, marsh plants, and seagrasses remain plentiful sources of new natural products, but ecological functions are known for only a small proportion of these compounds. As new analytical techniques are incorporated into ecological studies, opportunities are emerging for chemical ecologists to test how subtle environmental cues affect the production and release of marine angiosperm chemical defenses or signaling molecules. Throughout this review, we point to areas for future study, highlighting opportunities for new directions in chemical ecology that will advance our understanding of ecological interactions in these valuable ecosystems.

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References

  • Abbas A, Josefson M, Nylund GM, Pavia H, Abrahamsson K (2012) Chemical images of marine bio-active compounds by surface enhanced Raman spectroscopy and transposed orthogonal partial least squares (T-OPLS). Anal Chim Acta 737:37–44

    PubMed  CAS  Google Scholar 

  • Agostini S, Desjobert JM, Pergent G (1998) Distribution of phenolic compounds in the seagrass Posidonia oceanica. Phytochemistry 48:611–617

    CAS  Google Scholar 

  • Ahmed AA, Balboul BAA, Scott AI, Williams HH, Miao B, Mabry TJ (1998) Eudesmane derivatives from Iva frutescens. Phytochemistry 47:411–413

    PubMed  CAS  Google Scholar 

  • Alongi DM (1987) The influence of mangrove derived tannins on intertidal meiobenthos in tropical estuaries. Oecologia 71:537–540

    Google Scholar 

  • Aly AH, Debbab A, Kjer J, Proksch P (2010) Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41:1–16

    Google Scholar 

  • Andras TD, Alexander TS, Gahlena A, Parry RM, Fernandez FM, Kubanek J, Wang MD, Hay ME (2012) Seaweed allelopathy against coral: surface distribution of a seaweed secondary metabolite by imaging mass spectrometry. J Chem Ecol 38:1203–1214

    PubMed  CAS  Google Scholar 

  • Appel HM (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552

    CAS  Google Scholar 

  • Aquino RS, Landeira-Fernandez AM, Valente AP, Andrade LR, Mourao PAS (2005) Occurrence of sulfated galactans in marine angiosperms: evolutionary implications. Glycobiology 15:11–20

    PubMed  CAS  Google Scholar 

  • Arnold TM, Targett NM (2002) Marine tannins: the importance of a mechanistic framework for predicting ecological roles. J Chem Ecol 28:1919–1934

    PubMed  CAS  Google Scholar 

  • Arnold TA, Tanner CE, Rothen M, Bullington J (2008) Wound-induced accumulations of condensed tannins in turtlegrass, Thalassia testudinum. Aquat Bot 89:27–33

    CAS  Google Scholar 

  • Arnold T, Mealey C, Leahey H, Miller AW, Hall-Spencer JM, Milazzo M, Maers K (2012) Ocean acidification and the loss of phenolic substances in marine plants. PLoS One 7

  • Arvedlund M, Takemura A (2006) The importance of chemical environmental cues for juvenile Lethrinus nebulosus Forsskal (Lethrinidae, Teleostei) when settling into their first benthic habitat. J Exp Mar Biol Ecol 338:112–122

    CAS  Google Scholar 

  • Asha KK, Mathew S, Lakshmanan PT (2012) Flavonoids and phenolic compounds in two mangrove species and their antioxidant property. Indian J Mar Sci 41:259–264

    CAS  Google Scholar 

  • Awaad AS (2006) Phenolic glycosides of Juncus acutus and its anti-eczematic activity. Chem Nat Compd 42:152–155

    CAS  Google Scholar 

  • Azuma H, Toyota M, Asakawa Y, Takaso T, Tobe H (2002) Floral scent chemistry of mangrove plants. J Plant Res 115:47–53

    PubMed  CAS  Google Scholar 

  • Baden DG (1989) Brevetoxins: unique polyether dinoflagellate toxins. FASEB J 3:1807–1817

    PubMed  CAS  Google Scholar 

  • Baden DG, Bourdelais AJ, Jacocks H, Michelliza S, Naar J (2005) Natural and derivative brevetoxins: historical background, multiplicity, and effects. Environ Health Persp 113:621–625

    CAS  Google Scholar 

  • Bains G, Kumar AS, Rudrappa T, Alff E, Hanson TE, Bais HP (2009) Native plant and microbial contributions to a negative plant-plant interaction. Plant Physiol 151:2145–2151

    PubMed  CAS  Google Scholar 

  • Ballesteros E, Martin D, Uriz MJ (1992) Biological activity of extracts from some mediterranean macrophytes. Bot Mar 35:481–485

    Google Scholar 

  • Barbehenn RV, Bumgarner SL, Roosen EF, Martin MM (2001) Antioxidant defenses in caterpillars: role of the ascorbate-recycling system in the midgut lumen. J Insect Physiol 47:349–357

    PubMed  CAS  Google Scholar 

  • Barlocher F, Newell SY (1994a) Growth of the salt marsh periwinkle Littoraria irrorata on fungal and cordgrass diets. Mar Biol 118:109–114

    Google Scholar 

  • Barlocher F, Newell SY (1994b) Phenolics and proteins affecting palatability of Spartina leaves to the gastropod Littoraria irrorata. PSZNI Mar Ecol 15:65–75

    Google Scholar 

  • Barlocher F, Arsuffi TL, Newell SY (1989a) Digestive enzymes of the saltmarsh periwinkle Littorina irrorata (Mollusca, Gastropoda). Oecologia 80:39–43

    PubMed  CAS  Google Scholar 

  • Barlocher F, Newell SY, Arsuffi TL (1989b) Digestion of Spartina alterniflora Loisel material with and without fungal constituents by the periwinkle Littorina irrorata Say (Mollusca, Gastropoda). J Exp Mar Biol Ecol 130:45–53

    Google Scholar 

  • Baun A, Jensen SD, Bjerg PL, Christensen TH, Nyholm N (2000) Toxicity of organic chemical pollution in groundwater downgradient of a landfill (Grindsted, Denmark). Environ Sci Technol 34:1647–1652

    CAS  Google Scholar 

  • Behery FAA, Metwally Naeem ZE, Maatooq GT, Abdelfattah Amer MM, Wen ZH, Sheu JH, Ahmed AF (2007) Phenanthrenoids from Juncus acutus L., new natural lipopolysaccharide-inducible nitric oxide synthase inhibitors. Chem Pharm Bull 55:1264–1266

    PubMed  CAS  Google Scholar 

  • Behery FAA, Naeem ZEM, Maatooq GT, Amer MMA, Ahmed AF (2013) A novel antioxidant phenanthrenoid dimer from Juncus acutus L. Nat Prod Res 27:155–63

    PubMed  CAS  Google Scholar 

  • Bergh O, Borsheim KY, Bratbak G, Heldal M (1989) High abundance of viruses found in aquatic environments. Nature 340:467–468

    PubMed  CAS  Google Scholar 

  • Bernard P, Pesando D (1989) Antibacterial and antifungal activity of extracts from the rhizomes of the Mediterranean seagrass Posidonia oceanica (L) Delile. Bot Mar 32:85–88

    Google Scholar 

  • Bertness MD (1991) Zonation of Spartina patens and Spartina alterniflora in a New England salt marsh. Ecology 72:138–148

    Google Scholar 

  • Bitam F, Ciavatta ML, Carbone M, Manzo E, Mollo E, Gavagnin M (2010) Chemical analysis of flavonoid constituents of the seagrass Halophila stipulacea: first finding of malonylated derivatives in marine phanerogams. Biochem Syst Ecol 38:686–690

    CAS  Google Scholar 

  • Bitam F, Ciavatta ML, Manzo E, Villani G, Gavagnin M (2012) The first record of neolignans from the marine phanerogam Posidonia oceanica. Phytochem Lett 5:696–699

    CAS  Google Scholar 

  • Boettcher AA, Targett NM (1996) Induction of metamorphosis in queen conch, Strombus gigas Linnaeus, larvae by cues associated with red algae from their nursery grounds. J Exp Mar Biol Ecol 196:29–52

    Google Scholar 

  • Bowdish TI, Stiling P (1998) The influence of salt and nitrogen on herbivore abundance: direct and indirect effects. Oecologia 113:400–405

    Google Scholar 

  • Buchsbaum R, Valiela I (1987) Variability in the chemistry of estuarine plants and its effect on feeding by Canada geese. Oecologia 73:146–153

    Google Scholar 

  • Buchsbaum R, Valiela I, Swain T (1984) The role of phenolic compounds and other plant constituents in feeding by Canada geese in a coastal marsh. Oecologia 63:343–349

    Google Scholar 

  • Buchsbaum R, Wilson J, Valiela I (1986) Digestibility of plant constituents by Canada geese and Atlantic brant. Ecology 67:386–393

    Google Scholar 

  • Buchsbaum RN, Short FT, Cheney DP (1990) Phenolic-nitrogen interactions in eelgrass, Zostera marina L—Possible implications for disease resistance. Aquat Bot 37:291–297

    CAS  Google Scholar 

  • Bundy JG, Davey MP, Viant MR (2009) Environmental metabolomics: a critical review and future perspectives. Metabolomics 5:3–21

    CAS  Google Scholar 

  • Camilleri J (1989) Leaf choice by crustaceans in a mangrove forest in Queensland. Mar Biol 102:453–459

    Google Scholar 

  • Cannac M, Ferrat L, Barboni T, Pergent G, Pasqualini V (2007) The influence of tissue handling on the flavonoid content of the aquatic plant Posidonia oceanica. J Chem Ecol 33:1083–1088

    PubMed  CAS  Google Scholar 

  • Cantrell CL, Lu TS, Fronczek FR, Fischer NH, Adams LB, Franzblau SG (1996) Antimycobacterial cycloartanes from Borrichia frutescens. J Nat Prod 59:1131–1136

    PubMed  CAS  Google Scholar 

  • Chapatwala KD, de la Cruz AA, Miles DH (1981) Anti-microbial activity of juncusol, a novel 9,10-dihydrophenanthrene from the marsh plant Juncus roemerianus. Life Sci 29:1997–2001

    PubMed  CAS  Google Scholar 

  • Chen JD, Qiu Y, Yang ZW, Lin P, Lin YM (2008) Dimeric diterpenes from the roots of the mangrove plant Ceriops tagal. Helv Chim Acta 91:2292–2298

    CAS  Google Scholar 

  • Chen XL, Liu HL, Li J, Xin GR, Guo YW (2011) Paracaseolide a, first alpha-alkylbutenolide dimer with an unusual tetraquinane Oxa-cage bislactone skeleton from chinese mangrove Sonneratia paracaseolaris. Org Lett 13:5032–5035

    PubMed  CAS  Google Scholar 

  • Chiussi R, Diaz H, Rittschof D, Forward RB (2001) Orientation of the hermit crab Clibanarius antillensis: effects of visual and chemical cues. J Crustacean Biol 21:593–605

    Google Scholar 

  • Cui J, Ouyang J, Deng Z, Lin W (2008) Structure elucidation of an unprecedented alkaloid and a new limonoid from Xylocarpus granatum. Magn Res Chem 46:894–897

    CAS  Google Scholar 

  • Cundell AM, Brown MS, Stanford R, Mitchell R (1979) Microbial degradation of Rhizophora mangle leaves immersed in the sea. Estuar Coast Mar Sci 9:281–286

    CAS  Google Scholar 

  • Cuny P, Serve L, Jupin H, Boudouresque CF (1995) Water soluble phenolic compounds of the marine phanerogam Posidonia oceanica in a Mediterranean area colonised by the introduced chlorophyte Caulerpa taxifolia. Aquat Bot 52:237–242

    CAS  Google Scholar 

  • Davis M, Stoner AW (1994) Trophic cues induce metamorphosis of queen conch larvae (Strombus gigas linnaeus). J Exp Mar Biol Ecol 180:83–102

    Google Scholar 

  • de Bose JL, Nevitt GA, Dittman AH (2010) Rapid communication: experimental evidence that juvenile pelagic jacks (Carangidae) respond behaviorally to DMSP. J Chem Ecol 36:326–328

    Google Scholar 

  • de la Cerda LD, Jose DV, Derezende CE, Francisco MCF, Wasserman JC, Martins JC (1986) Leaf chemical characteristics affecting herbivory in a New World mangrove forest. Biotropica 18:350–355

    Google Scholar 

  • de la Cruz AA, Miles DH, Chapatwala KD (1982) Toxic effects of juncusol, a marsh plant phenolic extract, on estuarine fish and shrimp. Life Sci 30:1805–1810

    PubMed  Google Scholar 

  • Deegan LA, Johnson DS, Warren RS, Peterson BJ, Fleeger JW, Fagherazzi S, Wollheim WM (2012) Coastal eutrophication as a driver of salt marsh loss. Nature 490:388–92

    PubMed  CAS  Google Scholar 

  • Degenhardt DC, Lincoln DE (2006) Volatile emissions from an odorous plant in response to herbivory and methyl jasmonate exposure. J Chem Ecol 32:725–743

    PubMed  CAS  Google Scholar 

  • Delgado G, Rios MY, Colin L, Garcia PE, Alvarez L (1992) Constituents of Borrichia frutescens. Fitoterapia 63:273–274

    Google Scholar 

  • Della Greca M, Fiorentino A, Monaco P, Pinto G, Pollio A, Previtera L (1996) Action of antialgal compounds from Juncus effusus L on Selenastrum capricornutum. J Chem Ecol 22:587–603

    CAS  Google Scholar 

  • Della Greca M, Fiorentino A, Isidori M, Monaco P, Zarrelli A (2000) Antialgal ent-labdane diterpenes from Ruppia maritima. Phytochemistry 55:909–913

    CAS  Google Scholar 

  • Della Greca M, Fiorentino A, Monaco P, Zarrelli A (2001) Two new polyhydroxylated sterols from Ruppia maritima. Nat Prod Lett 15:111–118

    CAS  Google Scholar 

  • Della Greca M, Fiorentino A, Isidori M, Lavorgna M, Monaco P, Previtera L, Zarrelli A (2002) Phenanthrenoids from the wetland Juncus acutus. Phytochemistry 60:633–638

    CAS  Google Scholar 

  • Della Greca M, Fiorentino A, Isidori M, Previtera L, Temussi F, Zarrellia A (2003) Benzocoumarins from the rhizomes of Juncus acutus. Tetrahedron 59:4821–4825

    CAS  Google Scholar 

  • Della Greca M, Isidori M, Lavorgna M, Monaco P, Previtera L, Zarrelli A (2004) Bioactivity of phenanthrenes from Juncus acutus on Selenastrum capricornutum. J Chem Ecol 30:867–879

    CAS  Google Scholar 

  • Della Greca M, Previtera L, Zarrelli A (2005) Dimeric phenanthrenoids from Juncus acutus. Nat Prod Res 19:69–74

    CAS  Google Scholar 

  • Denno RF, Peterson MA, Gratton C, Cheng JA, Langellotto GA, Huberty AF, Finke DL (2000) Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores. Ecology 81:1814–1827

    Google Scholar 

  • Denno RF, Gratton C, Peterson MA, Langellotto GA, Finke DL, Huberty AF (2002) Bottom-up forces mediate natural-enemy impact in a phytophagous insect community. Ecology 83:1443–1458

    Google Scholar 

  • Devi P, Solimabi W, Dsouza L, Sonak S, Kamat SY, Singbal SYS (1997) Screening of some marine plants for activity against marine fouling bacteria. Bot Mar 40:87–91

    Google Scholar 

  • Diaz H, Orihuela B, Forward RB, Rittschof D (1999) Orientation of blue crab, Callinectes sapidus (Rathbun), megalopae: responses to visual and chemical cues. J Exp Mar Biol Ecol 233:25–40

    Google Scholar 

  • Diaz H, Orihuela B, Forward RB, Rittschof D (2001) Effects of chemical cues on visual orientation of juvenile blue crabs, Callinectes sapidus (Rathbun). J Exp Mar Biol Ecol 266:1–15

    CAS  Google Scholar 

  • Diaz H, Orihuela B, Forward RB, Rittschof D (2003) Orientation of juvenile blue crabs, Callinectes sapidus rathbun, to currents, chemicals, and visual cues. J Crustacean Biol 23:15–22

    Google Scholar 

  • Dicke M, Sabelis MW, Takabayashi J, Bruin J, Posthumus MA (1990) Plant strategies of manipulating predator–prey interactions through allelochemicals: prospects for application in pest control. J Chem Ecol 16:3091–3118

    CAS  Google Scholar 

  • Dudt JF, Shure DJ (1994) The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology 75:86–98

    Google Scholar 

  • Dumay O, Costa J, Desjobert JM, Pergent G (2004) Variations in the concentration of phenolic compounds in the seagrass Posidonia oceanica under conditions of competition. Phytochemistry 65:3211–3220

    PubMed  CAS  Google Scholar 

  • Emery NC, Ewanchuk PJ, Bertness MD (2001) Competition and salt marsh plant zonation: stress tolerators may be dominant competitors. Ecology 82:2471–2485

    Google Scholar 

  • Engel S, Jensen PR, Fenical W (2002) Chemical ecology of marine microbial defense. J Chem Ecol 28:1971–1985

    PubMed  CAS  Google Scholar 

  • Engel S, Puglisi MP, Jensen PR, Fenical W (2006) Antimicrobial activities of extracts from tropical atlantic marine plants against marine pathogens and saprophytes. Mar Biol 149:991–1002

    Google Scholar 

  • Erickson AA, Bell SS, Dawes CJ (2004) Does mangrove leaf chemistry help explain crab herbivory patterns? Biotropica 36:333–343

    Google Scholar 

  • Fauvel MT, Bousquetmelou A, Moulis C, Gleye J, Jensen SR (1995) Iridoid glucosides from Avicennia germinans. Phytochemistry 38:893–894

    CAS  Google Scholar 

  • Fauvel MT, Moulis C, Bon M, Fouraste I (1997) A new iridoid glucoside from African Avicennia germinans. Nat Prod Lett 10:139–142

    CAS  Google Scholar 

  • Fauvel MT, Bon M, Crasnier F, Moulis C, Fouraste I (1999) Megastigmane and iridoid glucosides from Avicennia germinans: two isomeric forms of an iridoid. Nat Prod Lett 14:99–106

    CAS  Google Scholar 

  • Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581

    Google Scholar 

  • Feeny P (1976) Plant apparancy and chemical defense. In: Wallace J, Mansell R (eds) Biochemical interactions between plants and insects. Plenum Press, New York, pp 1–40

    Google Scholar 

  • 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

    Google Scholar 

  • Fleck J, Fitt WK, Hahn MG (1999) A proline-rich peptide originating from decomposing mangrove leaves is one natural metamorphic cue of the tropical jellyfish Cassiopea xamachana. Mar Ecol Prog Ser 183:115–124

    CAS  Google Scholar 

  • Flewelling LJ (2008) Vectors of brevetoxins to marine mammals. Ph.D. Dissertation. University of South Florida, Tampa, p 144

    Google Scholar 

  • Flewelling LJ, Naar JP, Abbott JP, Baden DG, Barros NB, Bossart GD, Bottein MYD, Hammond DG, Haubold EM, Heil CA et al (2005) Red tides and marine mammal mortalities. Nature 435:755–756

    PubMed  CAS  Google Scholar 

  • Folin O, Ciocalteu V (1927) On tyrosine and tryptophane determinations in proteins. J Biol Chem 73:627–650

    Google Scholar 

  • Forward RB, Frankel DAZ, Rittschof D (1994) Molting of megalopae from the blue crab Callinectes sapidus—effects of offshore and estuarine cues. Mar Ecol Prog Ser 113:55–59

    Google Scholar 

  • Forward RB, 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

    Google Scholar 

  • Forward RB, Tankersley RA, Smith KA, Welch JM (2003) Effect of chemical cues on orientation of blue crab, Callinectes sapidus megalopae in flow: implications for location of nursery areas. Mar Biol 142:747–756

    Google Scholar 

  • Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–548

    PubMed  CAS  Google Scholar 

  • Gedan KB, Silliman BR, Bertness MD (2009) Centuries of human-driven change in salt marsh ecosystems. Annu Rev Mar Sci 1:117–141

    Google Scholar 

  • Geslin M, Verbist JF (1985) Flavonoids from Salicornia europaea. J Nat Prod 48:111–113

    CAS  Google Scholar 

  • Giddins RL, Lucas JS, Neilson MJ, Richards GN (1986) Feeding ecology of the mangrove crab Neosarmatium smithi (Crustacea, Decapoda, Sesarmidae). Mar Ecol Prog Ser 33:147–155

    Google Scholar 

  • Gillan FT, Hogg RW, Drew EA (1984) The sterol and fatty acid compositions of seven tropical seagrasses from North Queensland, Australia. Phytochemistry 23:2817–2821

    CAS  Google Scholar 

  • Goecke F, Labes A, Wiese J, Imhoff JF (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267–299

    CAS  Google Scholar 

  • Goecker ME, Heck KL, Valentine JF (2005) Effects of nitrogen concentrations in turtlegrass Thalassia testudinum on consumption by the bucktooth parrotfish Sparisoma radians. Mar Ecol Prog Ser 286:239–248

    Google Scholar 

  • Gopal B, Goel U (1993) Competition and allelopathy in aquatic plant communities. Bot Rev 59:155–210

    Google Scholar 

  • Goranson CE, Ho CK, Pennings SC (2004) Environmental gradients and herbivore feeding preferences in coastal salt marshes. Oecologia 140:591–600

    PubMed  Google Scholar 

  • Grosholz E (2010) Avoidance by grazers facilitates spread of an invasive hybrid plant. Ecol Lett 13:145–153

    PubMed  CAS  Google Scholar 

  • Gross EM (2003) Allelopathy of aquatic autotrophs. Crit Rev Plant Sci 22:313–339

    Google Scholar 

  • Guo HY, Pennings SC (2012) Mechanisms mediating plant distributions across estuarine landscapes in a low-latitude tidal estuary. Ecology 93:90–100

    PubMed  Google Scholar 

  • Haddad RI, Newell SY, Martens CS, Fallon RD (1992) Early diagenesis of lignin-associated phenolics in the salt marsh grass Spartina alterniflora. Geochim Cosmochim Ac 56:3751–3764

    CAS  Google Scholar 

  • Han L, Huang XS, Dahse HM, Moellmann U, Fu HZ, Grabley S, Sattler I, Lin WH (2007) Unusual naphthoquinone derivatives from the twigs of Avicennia marina. J Nat Prod 70:923–927

    PubMed  CAS  Google Scholar 

  • Han L, Huang X, Dahse HM, Moellmann U, Grabley S, Lin W, Sattler I (2008) New abietane diterpenoids from the mangrove Avicennia marina. Planta Medica 74:432–437

    PubMed  CAS  Google Scholar 

  • Harrison PG (1982) Control of microbial growth and of amphipod grazing by water-soluble compounds from leaves of Zostera marina. Mar Biol 67:225–230

    Google Scholar 

  • Harrison PG, Chan AT (1980) Inhibition of the growth of microalgae and bacteria by extracts of eelgrass (Zostera marina). Mar Biol 61:21–26

    Google Scholar 

  • Harrison PG, Durance CD (1985) Reductions in photosynthetic carbon uptake in epiphytic diatoms by water-soluble extracts of leaves of Zostera marina. Mar Biol 90:117–119

    CAS  Google Scholar 

  • Harrison PG, Durance C (1989) Seasonal variation in phenolic content of eelgrass shoots. Aquat Bot 35:409–413

    CAS  Google Scholar 

  • Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal J, Berenbaum M (eds) Herbivores: their interaction with secondary metabolites, evolutionary and ecological processes. Academic, San Diego, pp 371–413

    Google Scholar 

  • Heck KL, Valentine JF (2006) Plant-herbivore interactions in seagrass meadows. J Exp Mar Biol Ecol 330:420–436

    Google Scholar 

  • Heglmeier A, Zidorn C (2010) Secondary metabolites of Posidonia oceanica (Posidoniaceae). Biochem Syst Ecol 38:964–970

    CAS  Google Scholar 

  • Hendricks LG, Mossop HE, Kicklighter CE (2011) Palatability and chemical defense of Phragmites australis to the marsh periwinkle snail Littoraria irrorata. J Chem Ecol 37:838–845

    PubMed  CAS  Google Scholar 

  • Hernes PJ, Benner R, Cowie GL, Goni MA, Bergamaschi BA, Hedges JI (2001) Tannin diagenesis in mangrove leaves from a tropical estuary: a novel molecular approach. Geochim Cosmochim Ac 65:3109–3122

    CAS  Google Scholar 

  • Herz W, Bhat SV, Sudarsan V (1972) Sesquiterpene lactones and flavones of Iva frutescens. Phytochemistry 11:1829–1831

    CAS  Google Scholar 

  • Hitchcock GL, Fourqurean JW, Drake JL, Mead RN, Heil CA (2012) Brevetoxin persistence in sediments and seagrass epiphytes of east Florida coastal waters. Harmful Algae 13:89–94

    CAS  Google Scholar 

  • Hogg RW, Gillan FT (1984) Fatty acids, sterols and hydrocarbons in the leaves from eleven species of mangrove. Phytochemistry 23:93–97

    CAS  Google Scholar 

  • Houghton RA (1985) The effect of mortality on estimates of net above ground production by Spartina alterniflora. Aquat Bot 22:121–132

    Google Scholar 

  • Hovel KA, Bartholomew A, Lipcius RN (2001) Rapidly entrainable tidal vertical migrations in the salt marsh snail Littoraria irrorata. Estuaries 24:808–816

    Google Scholar 

  • Howes BL, Dacey JWH, Goehringer DD (1986) Factors controlling the growth form of Spartina alterniflora: feedbacks between above ground production, sediment oxidation, nitrogen and salinity. J Ecol 74:881–898

    Google Scholar 

  • Hu WM, Li MY, Li J, Xiao Q, Feng G, Wu J (2010) Dolabranes from the Chinese mangrove, Ceriops tagal. J Nat Prod 73:1701–1705

    CAS  Google Scholar 

  • Hueckelhoven R, Dechert C, Kogel KH (2001) Non-host resistance of barley is associated with a hydrogen peroxide burst at sites of attempted penetration by wheat powdery mildew fungus. Mol Plant Pathol 2:199–205

    Google Scholar 

  • Hughes AR (2012) A neighboring plant species creates associational refuge for consumer and host. Ecology 93:1411–1420

    PubMed  Google Scholar 

  • Huijbers CM, Mollee EM, Nagelkerken I (2008) Post-larval French grunts (Haemulon flavolineatum) distinguish between seagrass, mangrove and coral reef water: implications for recognition of potential nursery habitats. J Exp Mar Biol Ecol 357:134–139

    Google Scholar 

  • Huijbers CM, Nagelkerken I, Lossbroek PAC, Schulten IE, Siegenthaler A, Holderied MW, Simpson SD (2012) A test of the senses: fish select novel habitats by responding to multiple cues. Ecology 93:46–55

    PubMed  Google Scholar 

  • Iverson RL, Nearhoof FL, Andreae MO (1989) Production of dimethylsulfonium propionate and dimethylsulfide by phytoplankton in estuarine and coastal waters. Limnol Oceanogr 34:53–67

    CAS  Google Scholar 

  • Jay M, Viricel MR (1980) Flavonoids from Phragmites australis leaves: definition of the polyphenol profile of the species. Phytochemistry 19:2627–2628

    CAS  Google Scholar 

  • Jensen PR, Jenkins KM, Porter D, Fenical W (1998) Evidence that a new antibiotic flavone glycoside chemically defends the sea grass Thalassia testudinum against zoosporic fungi. Appl Environ Microb 64:1490–1496

    CAS  Google Scholar 

  • Kagan J, Mabry TJ (1969) Isorhamnetin 3-O-rutinoside flavonoid pigment in Batis maritima. Phytochemistry 8:325–326

    CAS  Google Scholar 

  • Kandil FE, Grace MH, Seigler DS, Cheeseman JM (2004) Polyphenolics in Rhizophora mangle L. leaves and their changes during leaf development and senescence. Trees-Struct Funct 18:518–528

    CAS  Google Scholar 

  • Kathiresan K (2003) Insect foliovory in mangroves. Indian J Mar Sci 32:237–239

    Google Scholar 

  • Kawasaki W, Matsui K, Akakabe Y, Itai N, Kajiwara T (1998) Volatiles from Zostera marina. Phytochemistry 47:27–29

    CAS  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144

    PubMed  CAS  Google Scholar 

  • Kiehn WM, Morris JT (2010) Variability in dimethylsulfoniopropionate (DMSP) concentrations in Spartina alterniflora and the effect on Littoraria irrorata. Mar Ecol Prog Ser 406:47–55

    Google Scholar 

  • Kimbro DL (2012) Tidal regime dictates the cascading consumptive and nonconsumptive effects of multiple predators on a marsh plant. Ecology 93:334–344

    PubMed  Google Scholar 

  • Kumar CS, Sarada DVL, Gideon TP, Rengasamy R (2008) Antibacterial activity of three South Indian seagrasses, Cymodocea serrulata, Halophila ovalis and Zostera capensis. World J Microb Biot 24:1989–1992

    Google Scholar 

  • Lane AL, Nyadong L, Galhena AS, Shearer TL, Stout EP, Parry RM, Kwasnik M, Wang MD, Hay ME, Fernandez FM et al (2009) Desorption electrospray ionization mass spectrometry reveals surface-mediated antifungal chemical defense of a tropical seaweed. Proc Nat Acad Sci USA 106:7314–7319

    PubMed  CAS  Google Scholar 

  • Lefebvre LW, Reid JP, Kenworthy WJ, Powell JA (2000) Characterizing manatee habitat use and seagrass grazing in Florida and Puerto Rico: implications for conservation and management. Pac Conserv Biol 5:289–298

    Google Scholar 

  • Li DL, Li XM, Wang BG (2008) Pentacyclic triterpenoids from the mangrove plant Rhizophora stylosa. Nat Prod Res 22:808–813

    PubMed  CAS  Google Scholar 

  • Li J, Li MY, Feng G, Xiao QA, Sinkkonen J, Satyanandamurty T, Wu J (2010) Limonoids from the seeds of a Godavari mangrove, Xylocarpus moluccensis. Phytochemistry 71:1917–1924

    PubMed  CAS  Google Scholar 

  • Li MY, Zhang J, Feng G, Satyanandamurty T, Wu J (2011) Khayasin and 2′ S-methylbutanoylproceranolide: promising candidate insecticides for the control of the coconut leaf beetle, Brontispa longissima. J Pest Sci 36:22–26

    Google Scholar 

  • Li J, Li MY, Feng G, Zhang J, Karonen M, Sinkkonen J, Satyanandamurty T, Wu J (2012a) Moluccensins R-Y, limonoids from the seeds of a Mangrove, Xylocarpus moluccensis. J Nat Prod 75:1277–1283

  • Li J, Li MY, Bruhn T, Goetz DCG, Xiao Q, Satyanandamurty T, Wu J, Bringmann G (2012b) Andhraxylocarpins A-E: structurally intriguing limonoids from the True Mangroves Xylocarpus granatum and Xylocarpus moluccensis. Chem-Eur J 18:14342–14351

  • Long J, Mitchell J, Sotka E (2011) Local consumers induce resistance differentially between Spartina populations in the field. Ecology 92:180–188

    PubMed  Google Scholar 

  • Luo J, Wang JS, Wang XB, Huang XF, Luo JG, Kong LY (2009) Chukvelutilides A-F, phragmalin limonoids from the stem barks of Chukrasia tabularis var. velutina. Tetrahedron 65:3425–3431

    CAS  Google Scholar 

  • Lytle JS, Lytle TF (2001) Use of plants for toxicity assessment of estuarine ecosystems. Environ Toxicol Chem 20:68–83

    PubMed  CAS  Google Scholar 

  • Mansour RMA, Zahran MA, Saleh NAM (1986) Flavonoids and ecology of Juncus acutus and Juncus rigidus in Egypt. Egypt J Bot 29–30:161–166

    Google Scholar 

  • Marczak LB, Ho CK, Wieski K, Vu H, Denno RF, Pennings SC (2011) Latitudinal variation in top-down and bottom-up control of a salt marsh food web. Ecology 92:276–281

    PubMed  CAS  Google Scholar 

  • McKee KL (1995) Interspecific variation in growth, biomass partitioning, and defensive characteristics of neotropical mangrove seedlings—response to light and nutrient availability. Am J Bot 82:299–307

    Google Scholar 

  • McKone KL, Tanner CE (2009) Role of salinity in the susceptibility of eelgrass Zostera marina to the wasting disease pathogen Labyrinthula zosterae. Mar Ecol Prog Ser 377:123–130

    CAS  Google Scholar 

  • McMillan C (1984) The condensed tannins (proanthocyanidins) in seagrasses. Aquat Bot 20:351–357

    CAS  Google Scholar 

  • McMillan C (1986) Sulfated flavonoids and leaf morphology in the Halophila ovalis H-minor complex (Hydrocharitaceae) of the Indo-Pacific Ocean. Aquat Bot 25:63–72

    CAS  Google Scholar 

  • McMillan C, Zapata O, Escobar L (1980) Sulfated phenolic compounds in seagrasses. Aquat Bot 8:267–278

    CAS  Google Scholar 

  • Meng Y, Krzysiak AJ, Durako MJ, Kunzelman JI, Wright JLC (2008) Flavones and flavone glycosides from Halophila johnsonii. Phytochemistry 69:2603–2608

    PubMed  CAS  Google Scholar 

  • Meyer KD, Paul VJ, Sanger HR, Nelson SG (1994) Effects of seaweed extracts and secondary metabolites on feeding by the herbivorous surgeonfish Naso lituratus. Coral Reefs 13:105–112

    Google Scholar 

  • Micheli F (1993) Feeding ecology of mangrove crabs in northeastern Australia—Mangrove litter consumption by Sesarma messa and Sesarma smithii. J Exp Mar Biol Ecol 171:165–186

    Google Scholar 

  • Miles DH, Mody NV, Minyard JP, Hedin PA (1973) Constituents of marsh grass: survey of the essential oils in Juncus roemerianus. Phytochemistry 12:1399–1404

    CAS  Google Scholar 

  • Miles DH, Randle S, Shakir R, Atwood JL (1981) Structure of juncunone: a biogenetically intriguing molecule from the marsh plant Juncus roemerianus. J Org Chem 46:2813–2815

    CAS  Google Scholar 

  • Moran KL, Bjorndal KA (2007) Simulated green turtle grazing affects nutrient composition of the seagrass Thalassia testudinum. Mar Biol 150:1083–1092

    CAS  Google Scholar 

  • Mozdzer TJ, Megonigal JP (2012) Jack-and-master trait responses to elevated CO2 and N: a comparison of native and introduced Phragmites australis. PLoS One 7

  • Mulderij G, Smolders AJP, van Donk E (2006) Allelopathic effect of the aquatic macrophyte, Stratiotes aloides, on natural phytoplankton. Freshwat Biol 51:554–561

    CAS  Google Scholar 

  • Nagelkerken I, Blaber SJM, Bouillon S, Green P, Haywood M, Kirton LG, Meynecke JO, Pawlik J, Penrose HM, Sasekumar A et al (2008) The habitat function of mangroves for terrestrial and marine fauna: a review. Aquat Bot 89:155–185

    Google Scholar 

  • Nawwar MAM, Elsissi HI, Baracat HH (1980) The flavonoids of Phragmites australis flowers. Phytochemistry 19:1854–1856

    CAS  Google Scholar 

  • Neilson MJ, Giddins RL, Richards GN (1986a) Effect of tannins on the palatability of mangrove leaves to the tropical sesarminid crab Neosarmatium smithii. Mar Ecol Prog Ser 34:185–186

    CAS  Google Scholar 

  • Neilson MJ, Painter TJ, Richards GN (1986b) Flavologlycan—a novel glycoconjugate from leaves of mangrove (Rhizophora stylosa Griff). Carbohyd Res 147:315–324

    CAS  Google Scholar 

  • Nevitt GA, Veit RR, Kareiva P (1995) Dimethyl sulfide as a foraging cue for Antarctic procellariiform seabirds. Nature 376:680–682

    CAS  Google Scholar 

  • Nishida N, Tamotsu S, Nagata N, Saito C, Sakai A (2005) Allelopathic effects of volatile monoterpenoids produced by Salvia leucophylla: inhibition of cell proliferation and DNA synthesis in the root apical meristem of Brassica campestris seedlings. J Chem Ecol 31:1187–1203

    PubMed  CAS  Google Scholar 

  • Nordhaus I, Wolff M (2007) Feeding ecology of the mangrove crab Ucides cordatus (Ocypodidae): food choice, food quality and assimilation efficiency. Mar Biol 151:1665–1681

    Google Scholar 

  • O’Connor NJ, Gregg AS (1998) Influence of potential habitat cues on duration of the megalopal stage of the fiddler crab Uca pugnax. J Crustacean Biol 18:700–709

    Google Scholar 

  • O’Connor NJ, Judge ML (1999) Cues in salt marshes stimulate molting of fiddler crab Uca pugnax megalopae: more evidence from field experiments. Mar Ecol Prog Ser 181:131–139

    Google Scholar 

  • O’Connor NJ, Judge ML (2004) Molting of fiddler crab Uca minax megalopae: stimulatory cues are specific to salt marshes. Mar Ecol Prog Ser 282:229–236

    Google Scholar 

  • Odum EP, de la Cruz AA (1967) Particulate organic detritus in a Georgia salt-marsh-estuarine ecosystem. In: Lauff GH (ed) Estuaries. AAAS, Washington, pp 383–388

    Google Scholar 

  • Olmstead KL, Denno RF, Morton TC, Romeo JT (1997) Influence of Prokelisia planthoppers on amino acid composition and growth of Spartina alterniflora. J Chem Ecol 23:303–321

    CAS  Google Scholar 

  • Olsen YS, Valiela I (2010) Effect of sediment nutrient enrichment and grazing on turtle grass Thalassia testudinum in jobos Bay, Puerto Rico. Estuar Coast 33:769–783

    CAS  Google Scholar 

  • Onuf CP, Teal JM, Valiela I (1977) Interactions of nutrients, plant growth, and herbivory in a mangrove ecosystem. Ecology 58:514–526

    Google Scholar 

  • Otte ML, Morris JT (1994) Dimethylsulphoniopropionate (DMSP) in Spartina alterniflora Loisel. Aquat Bot 48:239–259

    CAS  Google Scholar 

  • Otte ML, Wilson G, Morris JT, Moran BM (2004) Dimethylsulphoniopropionate (DMSP) and related compounds in higher plants. J Exp Bot 55:1919–1925

    PubMed  CAS  Google Scholar 

  • Pan JY, Chen SL, Li MY, Li J, Yang MH, Wu J (2010) Limonoids from the seeds of a hainan mangrove, Xylocarpus granatum. J Nat Prod 73:1672–1679

    CAS  Google Scholar 

  • Paul VJ, Nelson SG, Sanger HR (1990) Feeding preferences of adult and juvenile rabbitfish Siganus argenteus in relation to chemical defenses of tropical seaweeds. Mar Ecol Prog Ser 60:23–34

    CAS  Google Scholar 

  • Paul VJ, Ritson-Williams R, Sharp K (2011) Marine chemical ecology in benthic environments. Nat Prod Rep 28:345–387

    PubMed  CAS  Google Scholar 

  • Pawlik JR (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr Mar Biol 30:273–335

    Google Scholar 

  • Pennings SC, Bertness MD (2001) Salt marsh communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 289–316

    Google Scholar 

  • Pennings SC, Silliman BR (2005) Linking biogeography and community ecology: latitudinal variation in plant-herbivore interaction strength. Ecology 86:2310–2319

    Google Scholar 

  • Pennings SC, Carefoot TH, Siska EL, Chase ME, Page TA (1998) Feeding preferences of a generalist salt-marsh crab: relative importance of multiple plant traits. Ecology 79:1968–1979

    Google Scholar 

  • Pennings SC, Siska EL, Bertness MD (2001) Latitudinal differences in plant palatability in Atlantic coast salt marshes. Ecology 82:1344–1359

    Google Scholar 

  • Pennings SC, Zimmer M, Dias N, Sprung M, Dave N, Ho C-K, Kunza A, McFarlin C, Mews M, Pfauder A (2007) Latitudinal variation in plant-herbivore interactions in European salt marshes. Oikos 116:543–549

    Google Scholar 

  • Pennings SC, Ho CK, Salgado CS, Wieski K, Dave N, Kunza AE, Wason EL (2009) Latitudinal variation in herbivore pressure in Atlantic coast salt marshes. Ecology 90:183–195

    PubMed  Google Scholar 

  • Pergent G, Boudouresque C-F, Dumay O, Pergent-Martini C, Wyllie-Echeverria S (2008) Competition between the invasive macrophyte Caulerpa taxifolia and the seagrass Posidonia oceanica: contrasting strategies. BMC Ecol 8:20

    PubMed  Google Scholar 

  • Pino JA, Regalado EL (2010) Volatile constituents of Thalassia testudinum banks ex konig leaves. J Essent Oil Res 22:421–423

    CAS  Google Scholar 

  • Poulson KL, Sieg RD, Prince EK, Kubanek J (2010) Allelopathic compounds of a red tide dinoflagellate have species-specific and context-dependent impacts on phytoplankton. Mar Ecol Prog Ser 416:69–78

    CAS  Google Scholar 

  • Prado P, Heck KL Jr (2011) Seagrass selection by omnivorous and herbivorous consumers: determining factors. Mar Ecol Prog Ser 429:45–55

    Google Scholar 

  • Prado P, Romero J, Alcoverro T (2010) Nutrient status, plant availability and seasonal forcing mediate fish herbivory in temperate seagrass beds. Mar Ecol Prog Ser 409:229–239

    Google Scholar 

  • Preen A (1995) Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing. Mar Ecol Prog Ser 124:201–213

    Google Scholar 

  • Puglisi MP, Engel S, Jensen PR, Fenical W (2007) Antimicrobial activities of extracts from indo-pacific marine plants against marine pathogens and saprophytes. Mar Biol 150:531–540

    Google Scholar 

  • Purushothaman KK, Sarada A, Saraswathy A, Connolly JD (1983) Sempervirenic acid, a diterpene acid from Solidago sempervirens. Phytochemistry 22:1042–1043

    CAS  Google Scholar 

  • Qi SH, Zhang S, Qian PY, Wang BG (2008) Antifeedant, antibacterial, and antilarval compounds from the South China Sea seagrass Enhalus acoroides. Bot Mar 51:441–447

    CAS  Google Scholar 

  • Qi SH, Huang LS, He F, Zhang S, Dong JD (2012) Phytochemical and chemotaxonomic investigation of seagrass Thalassia hemprichii (Ehrenb.) Aschers (Hydrocharitaceae). Biochem Syst Ecol 43:128–131

    CAS  Google Scholar 

  • Quackenbush RC, Bunn D, Lingren W (1986) HPLC determination of phenolic acids in the water-soluble extract of Zostera marina L (eelgrass). Aquat Bot 24:83–89

    CAS  Google Scholar 

  • Raghukumar S (2002) Ecology of the marine protists, the Labyrinthulomycetes (Thraustochytrids and Labyrinthulids). Eur J Protistol 38:127–145

    Google Scholar 

  • Rahman YJ, Forward RB, Rittschof D (2000) Responses of mud snails and periwinkles to environmental odors and disaccharide mimics of fish odor. J Chem Ecol 26:679–696

    CAS  Google Scholar 

  • Ralph PJ, Short FT (2002) Impact of the wasting disease pathogen, Labyrinthula zosterae, on the photobiology of eelgrass Zostera marina. Mar Ecol Prog Ser 226:265–271

    Google Scholar 

  • Rasher DB, Stout EP, Engel S, Kubanek J, Hay ME (2011) Macroalgal terpenes function as allelopathic agents against reef corals. Proc Nat Acad Sci USA 108:17726–17731

    PubMed  CAS  Google Scholar 

  • Rashid MH, Asaeda T, Uddin MN (2010) The allelopathic potential of kudzu (Pueraria montana). Weed Sci 58:47–55

    CAS  Google Scholar 

  • Ravangpai W, Sommit D, Teerawatananond T, Sinpranee N, Palaga T, Pengpreecha S, Muangsin N, Pudhom K (2011) Limonoids from seeds of Thai Xylocarpus moluccensis. Bioorg Med Chem Lett 21:4485–4489

    PubMed  CAS  Google Scholar 

  • Regel RH, Ferris JM, Ganf GG, Brookes JD (2002) Algal esterase activity as a biomeasure of environmental degradation in a freshwater creek. Aquat Toxicol 59:209–223

    PubMed  CAS  Google Scholar 

  • Reinheimer G (1992) Aquatic microbiology. Wiley, New York

    Google Scholar 

  • Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126:444–450

    Google Scholar 

  • Rietsma CS, Valiela I, Sylvester-Serianni A (1982) Food preferences of dominant salt marsh herbivores and detritivores. Mar Ecol 3:179–189

    Google Scholar 

  • Rietsma CS, Valiela I, Buchsbaum R (1988) Detrital chemistry, growth, and food choice in the salt marsh snail (Melampus bidentatus). Ecology 69:261–266

    Google Scholar 

  • Riipi M, Ossipov V, Lempa K, Haukioja E, Koricheva J, Ossipova S, Pihlaja K (2002) Seasonal changes in birch leaf chemistry: are there trade-offs between leaf growth, and accumulation of phenolics? Oecologia 130:380–390

    Google Scholar 

  • Robblee MB, Barber TR, Carlson PR, Durako MJ, Fourqurean JW, Muehlstein LK, Porter D, Yarbro LA, Zieman RT, Zieman JC (1991) Mass mortality of the tropical seagrass Thalassia testudinum in Florida Bay (USA). Mar Ecol Prog Ser 71:297–299

    Google Scholar 

  • Robertson AI (1988) Decomposition of mangrove leaf litter in tropical Australia. J Exp Mar Biol Ecol 116:235–247

    Google Scholar 

  • Ross C, Puglisi MP, Paul VJ (2008) Antifungal defenses of seagrasses from the Indian River Lagoon. Florida Aquat Bot 88:134–141

    CAS  Google Scholar 

  • Rossi AM, Brodbeck BV, Strong DR (1996) Response of xylem-feeding leafhopper to host plant species and plant quality. J Chem Ecol 22:653–671

    CAS  Google Scholar 

  • Rowley DC, Hansen MST, Rhodes D, Sotriffer CA, Ni HH, McCammon JA, Bushman FD, Fenical W (2002) Thalassiolins A-C: new marine-derived inhibitors of HIV cDNA integrase. Bioorg Med Chem 10:3619–3625

    PubMed  CAS  Google Scholar 

  • Rudrappa T, Bonsall J, Bais HP (2007) Root-secreted allelochemical in the noxious weed Phragmites australis deploys a reactive oxygen species response and microtubule assembly disruption to execute rhizotoxicity. J Chem Ecol 33:1898–1918

    PubMed  CAS  Google Scholar 

  • Sala NM, Bertness MD, Silliman BR (2008) The dynamics of bottom-up and top-down control in a New England salt marsh. Oikos 117:1050–1056

    Google Scholar 

  • Salgado CS, Pennings SC (2005) Latitudinal variation in palatability of salt-marsh plants: are differences constitutive? Ecology 86:1571–1579

    Google Scholar 

  • Salminen JP, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338

    Google Scholar 

  • Salminen JP, Karonen M, Sinkkonen J (2011) Chemical ecology of tannins: recent developments in tannin chemistry reveal new structures and structure-activity patterns. Chem-Eur J 17:2806–2816

    PubMed  CAS  Google Scholar 

  • Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Nat Acad Sci USA 99:2445–2449

    PubMed  CAS  Google Scholar 

  • Sand-Jensen K (1977) Effect of epiphytes on eelgrass photosynthesis. Aquat Bot 3:55–63

    CAS  Google Scholar 

  • Sanina NM, Goncharova SN, Kostetsky EY (2004) Fatty acid composition of individual polar lipid classes from marine macrophytes. Phytochemistry 65:721–730

    PubMed  CAS  Google Scholar 

  • Sanina NM, Goncharova SN, Kostetsky EY (2008) Seasonal changes of fatty acid composition and thermotropic behavior of polar lipids from marine macrophytes. Phytochemistry 69:1517–1527

    Google Scholar 

  • Sarkar H, Zerezghi M, Bhattacharyya J (1988) Dehydrojuncusol, a constituent of the roots of Juncus roemerianus. Phytochemistry 27:3006–3008

    CAS  Google Scholar 

  • Sawabe T, Makino H, Tatsumi M, Nakano K, Tajima K, Iqbal MM, Yumoto I, Ezura Y, Christen R (1998) Pseudoalteromonas bacteriolytica sp. nov., a marine bacterium that is the causative agent of red spot disease of Laminaria japonica. Int J Syst Bacteriol 48:769–774

    PubMed  CAS  Google Scholar 

  • Schubauer JP, Hopkinson CS (1984) Aboveground and belowground emergent macrophyte production and turnover in a coastal marsh ecosystem. Georgia Limnol Oceanogr 29:1052–1065

    Google Scholar 

  • Shi C, Xu MJ, Bayer M, Deng ZW, Kubbutat MHG, Waejen W, Proksch P, Lin WH (2010) Phenolic compounds and their anti-oxidative properties and protein kinase inhibition from the Chinese mangrove plant Laguncularia racemosa. Phytochemistry 71:435–442

    PubMed  CAS  Google Scholar 

  • Short FT, Ibelings BW, Denhartog C (1988) Comparison of a current eelgrass disease to the wasting disease in the 1930s. Aquat Bot 30:295–304

    Google Scholar 

  • Sica D, Piccialli V, Masullo A (1984) Configuration at C-24 of sterols from the marine phanerogames Posidonia oceanica and Cymodocea nodosa. Phytochemistry 23:2609–2611

    CAS  Google Scholar 

  • Sieg RD, Willey D, Wolfe K, Kubanek J (2014a) Multiple chemical defenses produced by Spartina alterniflora deter farming snails and their fungal crop. Mar Ecol Prog Ser (in press)

  • Sieg RD, Wolfe K, Willey D, Ortiz-Santiago VM and Kubanek J (2014b) Chemical defenses against grazers and fungi limit establishment of fungal farms on salt marsh angiosperms. J Exp Mar Biol Ecol (in press)

  • Silliman BR, Bertness MD (2002) A trophic cascade regulates salt marsh primary production. Proc Nat Acad Sci USA 99:10500–10505

    PubMed  CAS  Google Scholar 

  • Silliman BR, Newell SY (2003) Fungal farming in a snail. Proc Nat Acad Sci USA 100:15643–15648

    PubMed  CAS  Google Scholar 

  • Silliman BR, Zieman JC (2001) Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology 82:2830–2845

    Google Scholar 

  • Silliman BR, van de Koppel J, Bertness MD, Stanton LE, Mendelssohn IA (2005) Drought, snails, and large-scale die-off of southern US salt marshes. Science 310:1803–1806

    PubMed  CAS  Google Scholar 

  • Siska EL, Pennings SC, Buck TL, Hanisak MD (2002) Latitudinal variation in palatability of salt-marsh plants: which traits are responsible? Ecology 83:3369–3381

    Google Scholar 

  • Skov MW, Hartnoll RG (2002) Paradoxical selective feeding on a low-nutrient diet: why do mangrove crabs eat leaves? Oecologia 131:1–7

    Google Scholar 

  • Smalley AE (1960) Energy flow of a salt marsh grasshopper population. Ecology 41:672–677

    Google Scholar 

  • Soltis DE, Bell CD, Kim S, Soltis PS (2008) Origin and early evolution of angiosperms. Ann NY Acad Sci 1133:3–25

    PubMed  CAS  Google Scholar 

  • Sotka EE, McCarty A, Monroe EA, Oakman N, van Dolah FM (2009) Benthic herbivores are not deterred by brevetoxins produced by the Red tide dinoflagellate Karenia brevis. J Chem Ecol 35:851–859

    PubMed  CAS  Google Scholar 

  • Steele L, Valentine JF (2012) Idiosyncratic responses of seagrass phenolic production following sea urchin grazing. Mar Ecol Prog Ser 466:81–92

    CAS  Google Scholar 

  • Steele L, Caldwell M, Boettcher A, Arnold T (2005) Seagrass-pathogen interactions: ‘Pseudo-induction’ of turtlegrass phenolics near wasting disease lesions. Mar Ecol Prog Ser 303:123–131

    Google Scholar 

  • Steinberg PD, de Nys R, Kjelleberg S (2002) Chemical cues for surface colonization. J Chem Ecol 28:1935–1951

    PubMed  CAS  Google Scholar 

  • Sun YQ, Guo YW (2004) Gymnorrhizol, an unusual macrocyclic polydisulfide from the Chinese mangrove Bruguiera gymnorrhiza. Tetrahedron Lett 45:5533–5535

    CAS  Google Scholar 

  • Sun Y, Jie O, Deng Z, Li Q, Lin W (2008) Structure elucidation of five new iridoid glucosides from the leaves of Avicennia marina. Magn Res Chem 46:638–642

    Google Scholar 

  • Tan QG, Luo XD (2011) Meliaceous limonoids: chemistry and biological activities. Chem Rev 111:7437–7522

    PubMed  CAS  Google Scholar 

  • Teal JM (1962) Energy flow in salt marsh ecosystem of Georgia. Ecology 43:614–624

    Google Scholar 

  • Todd JS, Zimmerman RC, Crews P, Alberte RS (1993) The antifouling activity of natural and synthetic phenolic acid sulfate esters. Phytochemistry 34:401–404

    CAS  Google Scholar 

  • Tomas F, Abbott JM, Steinberg C, Balk M, Williams SL, Stachowicz JJ (2011) Plant genotype and nitrogen loading influence seagrass productivity, biochemistry, and plant-herbivore interactions. Ecology 92:1807–1817

    PubMed  CAS  Google Scholar 

  • Turner IM (1995) Foliar defenses and habitat adversity of 3 woody plant communities in Singapore. Funct Ecol 9:279–284

    Google Scholar 

  • Valiela I, Rietsma CS (1984) Nitrogen, phenolic acids, and other feeding cues for salt marsh detritivores. Oecologia 63:350–356

    Google Scholar 

  • Valiela I, Koumjian L, Swain T, Teal JM, Hobbie JE (1979) Cinnamic acid inhibition of detritus feeding. Nature 280:55–57

    CAS  Google Scholar 

  • Valiela I, Wilson J, Buchsbaum R, Rietsma C, Bryant D, Foreman K, Teal J (1984) Importance of chemical composition of salt marsh litter on decay rates and feeding by detritivores. Bull Mar Sci 35:261–269

    Google Scholar 

  • Vergeer LHT, Develi A (1997) Phenolic acids in healthy and infected leaves of Zostera marina and their growth-limiting properties towards Labyrinthula zosterae. Aquat Bot 58:65–72

    CAS  Google Scholar 

  • Vergeer LHT, Aarts TL, Degroot JD (1995) The wasting disease and the effect of abiotic factors (light intensity, temperature, salinity) and infection with Labyrinthula zosterae on the phenolic content of Zostera marina shoots. Aquat Bot 52:35–44

    CAS  Google Scholar 

  • Verges A, Becerro MA, Alcoverro T, Romero J (2007a) Experimental evidence of chemical deterrence against multiple herbivores in the seagrass Posidonia oceanica. Mar Ecol Prog Ser 343:107–114

    CAS  Google Scholar 

  • Verges A, Becerro MA, Alcoverro T, Romero J (2007b) Variation in multiple traits of vegetative and reproductive seagrass tissues influences plant-herbivore interactions. Oecologia 151:675–686

    PubMed  Google Scholar 

  • Verges A, Perez M, Alcoverro T, Romero J (2008) Compensation and resistance to herbivory in seagrasses: induced responses to simulated consumption by fish. Oecologia 155:751–760

    PubMed  Google Scholar 

  • Verges A, Alcoverro T, Romero J (2011) Plant defences and the role of epibiosis in mediating within-plant feeding choices of seagrass consumers. Oecologia 166:381–390

    PubMed  Google Scholar 

  • Vervoort HC, Pawlik JR, Fenical W (1998) Chemical defense of the caribbean ascidian Didemnum conchyliatum. Mar Ecol Prog Ser 164:221–228

    CAS  Google Scholar 

  • Wahl M, Hay ME (1995) Associational resistance and shared doom: effects of epibiosis on herbivory. Oecologia 102:329–340

    Google Scholar 

  • Wang YG, Wang YL, Zhai HF, Liao YJ, Zhang B, Huang JM (2012) Phenanthrenes from Juncus effusus with anxiolytic and sedative activities. Nat Prod Res 26:1234–1239

    PubMed  CAS  Google Scholar 

  • Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL Jr, Hughes AR (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Nat Acad Sci USA 106:12377–12381

    PubMed  CAS  Google Scholar 

  • Weidenhamer JD, Li M, Allman J, Bergosh RG, Posner M (2013) Evidence does not support a role for gallic acid in Phragmites australis invasion success. J Chem Ecol 39:323–32

    PubMed  CAS  Google Scholar 

  • Welch JM, Rittschof D, Bullock TM, Forward RB (1997) Effects of chemical cues on settlement behavior of blue crab Callinectes sapidus postlarvae. Mar Ecol Prog Ser 154:143–153

    Google Scholar 

  • Williams SL, Ruckelshaus MH (1993) Effects of nitrogen availability and herbivory on eelgrass (Zostera marina) and epiphytes. Ecology 74:904–918

    Google Scholar 

  • Wissler L, Codoner FM, Gu J, Reusch TBH, Olsen JL, Procaccini G, Bornberg-Bauer E (2011) Back to the sea twice: identifying candidate plant genes for molecular evolution to marine life. BMC Evol Biol 11

  • Wu J, Xiao Q, Xu J, Li MY, Pan JY, Yang MH (2008a) Natural products from true mangrove flora: source, chemistry and bioactivities. Nat Prod Rep 25:955–981

    PubMed  CAS  Google Scholar 

  • Wu J, Zhang S, Bruhn T, Xiao Q, Ding HX, Bringmann G (2008b) Xylogranatins F-R: antifeedants from the chinese mangrove, Xylocarpus granatum, a new biogenetic pathway to tetranortriterpenoids. Chem-Eur J 14:1129–1144

    PubMed  CAS  Google Scholar 

  • Yin S, Fan CQ, Wang XN, Lin LP, Ding J, Yue JM (2006) Xylogranatins A-D: novel tetranortriterpenoids with an unusual 9,10-seco scaffold from marine mangrove Xylocarpus granatum. Org Lett 8:4935–4938

    PubMed  CAS  Google Scholar 

  • Zapata O, McMillan C (1979) Phenolic acids in seagrasses. Aquat Bot 7:307–317

    CAS  Google Scholar 

  • Zimmer M, Danko JP, Pennings SC, Danford AR, Carefoot TH, Ziegler A, Uglow RF (2002) Cellulose digestion and phenol oxidation in coastal isopods (Crustacea: Isopoda). Mar Biol 140:1207–1213

    CAS  Google Scholar 

  • Zimmer M, Pennings SC, Buck TL, Carefoot TH (2004) Salt marsh litter and detritivores: a closer look at redundancy. Estuaries 27:753–769

    Google Scholar 

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Acknowledgments

The authors thank Kelsey Poulson-Ellestad, Melanie Heckman, and two anonymous reviewers for suggestions that improved the manuscript. NSF grants OCE-1060300 and NSF REU Site Award OCE-0851606, as well as a US Department of Education GAANN fellowship awarded to RDS, has supported our recent research in marine chemical ecology.

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Correspondence to Julia Kubanek.

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Julia Kubanek: 2012 ISCE Silverstein-Simeone Lecture Award recipient

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Sieg, R.D., Kubanek, J. Chemical Ecology of Marine Angiosperms: Opportunities at the Interface of Marine and Terrestrial Systems. J Chem Ecol 39, 687–711 (2013). https://doi.org/10.1007/s10886-013-0297-9

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  • DOI: https://doi.org/10.1007/s10886-013-0297-9

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