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Anti-grazing activity and seasonal variation of dimethylsulfoniopropionate-associated compounds in the invasive alga Codium fragile ssp. tomentosoides

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Abstract

In this study, we present evidence that the invasive alga Codium fragile ssp. tomentosoides is chemically defended against grazing by a wound-activated chemical defense involving dimethylsulfoniopropionate (DMSP) and the products of its cleavage, dimethylsulfide (DMS), and acrylic acid (AA). DMSP in C. fragile ssp. tomentosoides was present throughout the year, but concentrations varied seasonally and were highest in the winter. Intra-thallus variation was neither large, nor consistent over time. High DMSP concentrations were uncommon among northwestern Atlantic macrophytes. Of 26 other species tested, only two, Ulva lactuca and Polysiphonia harveyi contained concentrations comparable to, or higher than, those of C. fragile ssp. tomentosoides. DMS and AA, both individually and together, deterred grazing by the green sea urchin Strongylocentrotus droebachiensis at “natural” concentrations. These results suggest that DMS and AA contribute to the avoidance of C. fragile ssp. tomentosoides by S. droebachiensis. As a result, the production of DMSP and its subsequent cleavage, upon injury, may reduce herbivory on C. fragile ssp. tomentosoides and contribute to its success.

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References

  • Amade P, Lemee R (1998) Chemical defence of the Mediterranean alga Caulerpa taxifolia: variations in caulerpenyne production. Aquat Toxicol 43:287–300

    Article  CAS  Google Scholar 

  • Benson EE, Rutter JC, Cobb AH (1983) Seasonal variation in frond morphology and chloroplast physiology of the intertidal alga Codium fragile (Suringar) Hariot. New Phyol 95:569–580

    Article  Google Scholar 

  • Bischoff B, Karsten U, Daniel C, Kuck K, Xia B, Wiencke C (1994) Preliminary assessment of the beta-dimethylsulfoniopropionate (DMSP) content of macroalgae from the tropical island Hainan (People’s Republic of China). Aust J Mar Freshw Res 45:1329–1336

    Article  CAS  Google Scholar 

  • Bouck GB, Morgan E (1957) The occurrence of Codium in Long Island waters. Bull Torrey Bot Club 84:384–387

    Article  Google Scholar 

  • Bricelj VM, Twarog BM, MacQuarrie SP, Chang P, Trainer VL (2000) Does the history of toxin exposure influence bivalve population responses to PSP toxins in Mya arenaria?: I) burrowing and nerve responses. J Shellfish Res 19:635

    Google Scholar 

  • Bricelj VM, Connell L, Konoki K, MacQuarrie SP, Scheuer T, Catterall WA, Trainer VL (2005) Sodium channel mutation leading to saxitoxin resistance in clams increases risk of PSP. Nature 434:763–767

    Article  PubMed  CAS  Google Scholar 

  • Bruno JF, O’Connor MI (2005) Cascading effects of predator diversity and omnivory in marine food webs. Ecol Lett 8:1048–1056

    Article  Google Scholar 

  • Castilla JC, Uribe M, Bahamonde N, Clarke M, Desqueyroux Faundez R, Kong I, Moyano H, Rozbaczylo N, Santelices B, Valdovinos C, Zavala P (2005) Down under the southeastern pacific: marine non-indigenous species in Chile. Biol Invasions 7:213–232

    Article  Google Scholar 

  • Chapman AS, Scheibling RE, Chapman ARO (2002) Species introductions and changes in marine vegetation of Atlantic Canada. In: Claudi R, Nantel P, Muckle-Jeffs E (eds) Alien invaders in Canada’s waters, wetlands and forests. Natural Resources Canada, Canadian Forest Service Science Branch, Ottawa, pp 133–148

    Google Scholar 

  • Chavanich S, Harris LG (2002) The influence of macroalgae on seasonal abundance and feeding preference of a subtidal snail, Lacuna vincta (Montagu) (Littorinidae) in the Gulf of Maine. J Molluscan Stud 68:73–78

    Article  Google Scholar 

  • Cronin G, Hay ME (1996a) Induction of seaweed chemical defenses by amphipod grazing. Ecology 77:2287–2301

    Article  Google Scholar 

  • Cronin G, Hay ME (1996b) Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology 77:1531–1543

    Article  Google Scholar 

  • Cruz-Rivera E, Hay ME (2003) Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol Monogr 73:483–506

    Article  Google Scholar 

  • Dethier MN, Williams SL, Freeman A (2005) Seaweeds under stress: manipulated stress and herbivory affect critical life-history functions. Ecol Monogr 75:403–418

    Article  Google Scholar 

  • Dromgoole FI (1975) Occurrence of Codium fragile subspecies tomentosoides in New Zealand waters. N Z J Mar Freshw Res 9:257–264

    Article  Google Scholar 

  • Duffy JE, Hay ME (1994) Herbivore resistance to seaweed chemical defense: the roles of mobility and predation risk. Ecology 75:1304–1319

    Article  Google Scholar 

  • Duffy JE, Paul VJ (1992) Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333–339

    Article  Google Scholar 

  • Dumay O, Pergent G, Pergent Martini C, Amade P (2002) Variations in caulerpenyne contents in Caulerpa taxifolia and Caulerpa racemosa. J Chem Ecol 28:343–352

    Article  PubMed  CAS  Google Scholar 

  • Edwards DM, Reed RH, Chudek JA, Foster R, Stewart WDP (1987) Organic solute accumulation in osmotically-stressed Enteromorpha intestinalis. Mar Biol 95:583–592

    Article  CAS  Google Scholar 

  • Edwards DM, Reed RH, Stewart WDP (1988) Osmoacclimation in Enteromorpha intestinalis: long-term effects of osmotic stress on organic solute accumulation. Mar Biol 88:457–476

    Google Scholar 

  • Fralick RA, Mathieson AC (1972) Winter fragmentation of Codium fragile (Suringar) Hariot ssp. tomentosoides (Van Goor) Silva (Chlorophyceae, Siphonales) in New England. Phycologia 11:67–70

    Google Scholar 

  • Harris LG, Tyrrell MC (2001) Changing community states in the Gulf of Maine: synergism between invaders, overfishing and climate change. Biol Invasions 3:9–21

    Article  Google Scholar 

  • Hay ME (1996) Marine chemical ecology: what’s known and what’s next? J Exp Mar Biol Ecol 200:103–134

    Article  CAS  Google Scholar 

  • Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145

    Article  Google Scholar 

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

    Google Scholar 

  • Hay ME, Kappel QE, Fenical AW (1994) Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 75:1714–1726

    Article  Google Scholar 

  • Hay ME, Duffy JE, Pfister CA, Fenical W (1987) Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology 68:1567–1580

    Article  CAS  Google Scholar 

  • Hay ME, Paul VJ, Lewis SM, Gustafson K, Tucker J, Trindell RN (1988) Can tropical seaweeds reduce herbivory by growing at night? Diel patterns of growth, nitrogen content, herbivory, and chemical versus morphological defenses. Oecologia 75:233–245

    Article  Google Scholar 

  • Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064

    Article  Google Scholar 

  • Karsten U, Wiencke C, Kirst GO (1992) Dimethylsulphoniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature. Polar Biol 12:603–607

    Article  Google Scholar 

  • Karsten U, Kück K, Vogt C, Kirst GO (1996) Dimethylsulfoniopropionate production in phototrophic organisms and its physiological function as a cryoprotectant. In: Kiene RP, Visscher P, Kirst G, Keller M (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds. Plenum, New York, pp 143–153

    Google Scholar 

  • Karsten U, Kueck K, Daniel C, Wiencke C, Kirst GO (1994) A method for complete determination of dimethylsulphoniopropionate (DMSP) in marine macroalgae from different geographical regions. Phycologia 33:171–176

    Google Scholar 

  • Kirst G (1989) Salinity tolerance of eukaryotic marine algae. Ann Rev Plant Physiol Plant Mol Biol 40:21–53

    Google Scholar 

  • Kirst GO, Thiel C, Wolff H, Nothnagel J, Wanzek M, Ulmke R (1991) Dimethylsulphoniopropionate (DMSP) in ice-algae and its possible biological role. Mar Chem 35:381–388

    Article  CAS  Google Scholar 

  • Levin PS, Coyer JA, Petrik R, Good TP (2002) Community-wide effects of non-indigenous species on temperate reefs. Ecology 83:3182–3193

    Google Scholar 

  • Lubchenco J (1978) Plant species diversity in a marine intertidal community: importance of herbivore food preference and algal competitive abilities. Am Nat 112:23–39

    Article  Google Scholar 

  • Lyons DA, Scheibling RE (2007) Differences in somatic and gonadic growth of sea urchins (Stronglyocentrotus droebachiensis) fed kelp (Laminaria longicruris) or the invasive alga Codium fragile ssp. tomentosoides are related to energy acquisition. Mar Biol 152:285–295

    Article  Google Scholar 

  • Macaya EC, Rothaeusler E, Thiel M, Molis M, Wahl M (2005) Induction of defenses and within-alga variation of palatability in two brown algae from the northern-central coast of Chile: effects of mesograzers and UV radiation. J Exp Mar Biol Ecol 325:214–227

    Article  Google Scholar 

  • MacQuarrie SP, Bricelj VM (2000) Does the history of toxin exposure influence bivalve population responses to PSP toxins in Mya arenaria?: II) feeding, survival and toxin accumulation. J Shellfish Res 19:636–637

    Google Scholar 

  • McIvor L, Maggs CA, Provan J, Stanhope MJ (2001) rbcL sequences reveal multiple cryptic introductions of the japanese red alga Polysiphonia harveyi. Mol Ecol 10:911–919

    Article  PubMed  CAS  Google Scholar 

  • Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461

    Article  PubMed  CAS  Google Scholar 

  • Pavia H, Toth GB (2000) Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212–3225

    Google Scholar 

  • Pavia H, Cervin G, Lindgren A, Aberg P (1997) Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar Ecol Prog Ser 157:139–146

    Article  CAS  Google Scholar 

  • Prince JS, LeBlanc WG (1992) Comparative feeding preference of Strongylocentrotus droebachiensis (Echinoidea) for the invasive seaweed Codium fragile ssp. tomentosoides (Chlorophyceae) and four other seaweeds. Mar Biol 113:159–163

    Article  Google Scholar 

  • Reed RH (1983) Measurement and osmotic significance of beta-dimethylsulfoniopropionate in marine macroalgae. Mar Biol Lett 4:173–181

    CAS  Google Scholar 

  • Renaud PE, Hay ME, Schmitt TM (1990) Interactions of plant stress and herbivory: intraspecific variation in the susceptibility of a palatable versus an unpalatable seaweed to sea urchin grazing. Oecologia 82:217–223

    Article  Google Scholar 

  • Ross C, Van Alstyne KL (2007) Intraspecific variation in stress-induced hydrogen peroxide scavenging by the ulvoid macroalga Ulva lactuca. J Phycol 43:466–474

    Article  Google Scholar 

  • Scheibling RE, Anthony SX (2001) Feeding, growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp. tomentosoides. Mar Biol 139:139–146

    Article  Google Scholar 

  • Scheibling RE, Gagnon P (2006) Competitive interactions between the invasive green alga Codium fragile ssp. tomentosoides and native canopy-forming seaweeds in Nova Scotia (Canada). Mar Ecol Prog Ser 325:1–14

    Article  Google Scholar 

  • Scheibling RE, Hatcher BG (2006) The ecology of Strongylocentrotus droebachiensis. In: Lawrence JM (eds) Edible sea urchins: biology and ecology, 2nd edn. Elsevier Science BV, Amsterdam, pp 353–392

    Google Scholar 

  • Silva PC (1955) The dichotomous species of Codium in Britain. J Mar Biol Assoc UK 34:565–577

    Article  Google Scholar 

  • Sotka EE (2003) Genetic control of feeding preference in the herbivorous amphipod Ampithoe longimana. Mar Eco Prog Ser 256:305–310

    Article  Google Scholar 

  • Sotka EE, Hay ME (2002) Geographic variation among herbivore populations in tolerance for a chemically rich seaweed. Ecology 83:2721–2735

    Google Scholar 

  • Sotka EE, Wares JP, Hay ME (2003) Geographic and genetic variation in feeding preference for chemically defended seaweeds. Evolution 57:2262–2276

    PubMed  Google Scholar 

  • Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res 43:183–197

    Article  CAS  Google Scholar 

  • Steinberg PD, Van AItena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222

    Article  Google Scholar 

  • Sumi CBT, Scheibling RE (2005) Role of grazing by sea urchins Strongylocentrotus droebachiensis in regulating the invasive alga Codium fragile ssp tomentosoides in Nova Scotia. Mar Ecol Prog Ser 292:203–212

    Article  Google Scholar 

  • Sunda W, Kieber DJ, Kiene RP, Huntsman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320

    Article  PubMed  CAS  Google Scholar 

  • Taylor RB, Sotka E, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76

    Article  Google Scholar 

  • Trowbridge CD (1995) Establishment of the green alga Codium fragile ssp. tomentosoides on New Zealand rocky shores: current distribution and invertebrate grazers. J Ecol 83:949–965

    Article  Google Scholar 

  • Trowbridge CD (1998) Ecology of the green macroalga Codium fragile (Suringar) Hariot 1889: invasive and non-invasive subspecies. Oceanogr Mar Biol Annu Rev 36:1–64

    Google Scholar 

  • Trowbridge CD (1999) An assessment of the potential spread and options for control of the introduced green macroalga Codium fragile ssp. tomentosoides on Australian shores. Consultancy report. CSIRO/Centre for Research on Introduced Marine Pests, Hobart

  • Trowbridge CD (2004) Emerging associations on marine rocky shores: specialist herbivores on introduced macroalgae. J Anim Ecol 73:294–308

    Article  Google Scholar 

  • Van Alstyne KL (1988) Herbivore grazing increases polyphenolic defenses in the brown alga Fucus distichus. Ecology 69:655–663

    Article  Google Scholar 

  • Van Alstyne KL, Houser LT (2003) Dimethylsulfide release during macroinvertebrate grazing and its role as an activated chemical defense. Mar Ecol Prog Ser 250:175–181

    Article  Google Scholar 

  • Van Alstyne KL, Puglisi MP (2007) DMSP in marine macroalgae and macroinvertebrates: distribution, functions, and ecological impacts. Aquat Sci. doi:10.1007/s00027-007-0888-z

    Google Scholar 

  • Van Alstyne KL, Dethier MN, Duggins DO (2003) Spatial patterns in macroalgal chemical defenses. In: McClintock J, Baker W (eds) Marine chemical ecology. CRC, Boca Raton, pp 301–324

    Google Scholar 

  • Van Alstyne KL, Koellermeier L, Nelson TA (2007) Spatial variation in dimethylsulfoniopropionate (DMSP) production in Ulva lactuca (Chlorophyta) from the northeast Pacific. Mar Biol 150:1127–1135

    Article  CAS  Google Scholar 

  • Van Alstyne KL, Nelson AV, Vyvyan JR, Cancilla D (2006) Dopamine functions as an antiherbivore defense in a “green tide” alga. Oecologia 248:304–311

    Article  Google Scholar 

  • Van Alstyne KL, Wolfe GV, Freidenburg TL, Neill A, Hicken C (2001) Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage. Mar Ecol Prog Ser 213:53–65

    Article  Google Scholar 

  • Van Donk E, Hessen DO (1995) Reduced digestibility of UV-B stressed and nutrient-limited algae by Daphnia magna. Hydrobiologia 307:147–151

    Article  Google Scholar 

  • Van Donk E, Hessen DO (1993) Grazing resistance in nutrient-stressed phytoplankton. Oecologia 93:508–511

    Article  Google Scholar 

  • Van Donk E, Lurling M, Hessen DO, Lokhorst GM (1997) Altered cell wall morphology in nutrient-deficient phytoplankton and its impact on grazers. Limnol Oceanogr 42:357–364

    Article  Google Scholar 

  • Wright JT, Dworjanyn SA, Rogers CN, Steinberg PD, Williamson JE, Poore AGB (2005) Density-dependent sea urchin grazing: differential removal of species, changes in community composition and alternative community states. Mar Ecol Prog Ser 298:143–156

    Article  Google Scholar 

  • Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757–1766

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River

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Acknowledgments

We thank O. D’Amours, P. Gagnon, J. Lindley, A. Pinder, M. Saunders, and A. Schmidt for their help in collecting algal samples. J-S. Lauzon-Guay, M. Auger-Méthé, and three anonymous reviewers provided valuable suggestions on the manuscript. This work was supported by NSERC Postgraduate and Killam Predoctoral Scholarships (to D.A.L.) and research grants from NSERC (to R.E.S.) and the National Science Foundation (OCE-0526644 and IOB-0090825, to K. L. V.).

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Authors and Affiliations

  1. Department of Biology, Dalhousie University, Halifax, NS, Canada, B3H 4J1

    Devin A. Lyons & Robert E. Scheibling

  2. Shannon Point Marine Center, Western Washington University, 1900 Shannon Point Road, Anacortes, WA, 98221, USA

    Kathryn L. Van Alstyne

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  1. Devin A. Lyons
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  2. Kathryn L. Van Alstyne
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Correspondence to Devin A. Lyons.

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Communicated by R.J. Thompson.

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Lyons, D.A., Van Alstyne, K.L. & Scheibling, R.E. Anti-grazing activity and seasonal variation of dimethylsulfoniopropionate-associated compounds in the invasive alga Codium fragile ssp. tomentosoides . Mar Biol 153, 179–188 (2007). https://doi.org/10.1007/s00227-007-0795-9

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