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Adaptation mechanisms and ecological consequences of seaweed invasions: a review case of agarophyte Gracilaria vermiculophylla

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Abstract

To prioritize management, conservation and restoration from seaweed invasions, it is important for policy-makers to elucidate the ecological mechanisms during the three phases of invasion: introduction, establishment, and diffusion. In this review, we synthesize the current knowledge of the invasion mechanisms and ecological impacts of Gracilaria vermiculophylla, a red agarophyte native to Asia Northwest Pacific, which now has become a rapid and successful coastal invader in the Atlantic and Eastern Pacific Oceans. Eco-physiological and chemical studies have revealed that some ecological traits, including survival in dark condition (e.g. the ballast water), tolerance to grazing and extreme salinities and temperatures, insensitive to UVR and light intensity and nutrient levels, adaptation to a wide diversity of habitats, and chemical defense to potential predators, may provide G. vermiculophylla an unmatched advantage during its global invasion. The rapid growth, flexible reproduction through fragmentation, efficient recruitment on hard substratum, seeding success on various vectors, and interaction with local community organisms may also contribute to its rapid increase in abundance and effects on the invaded coastal ecosystems. G. vermiculophylla showed both negative and positive impacts to the marine ecosystems through changing interspecific competition, increasing habitat diversity, altering the community complex, and transforming biogeochemical cycles and estuarine food webs. Future surveys such as marine exotic genomics, transcriptome sequencing and epigenetic variation between native and invasive entities may provide insightful promise on molecular mechanisms of seaweed invasion.

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References

  • Abreu MH, Pereira R, Sousa-Pinto I, Yarish C (2011a) Nitrogen uptake response of Gracilaria vermiculophylla (Ohmi) Papenfuss under combined and single addition of nitrate and ammonium. J Exp Mar Biol Ecol 407:190–199

    Article  CAS  Google Scholar 

  • Abreu MH, Pereira R, Sousa-Pinto I, Yarish C (2011b) Ecophysiological studies of the non-indigenous species Gracilaria vermiculophylla (Rhodophyta) and its abundance patterns in Ria de Aveiro lagoon, Portugal. Eur J Phycol 46:453–464

    Article  Google Scholar 

  • Adam P (1990) Salt marsh ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Auffrey LM, Robinson SMC, Barbeau MA (2004) Effect of green macroalgal mats on burial depth of soft-shelled clams Mya arenaria. Mar Ecol Prof Ser 278:193–203

    Article  Google Scholar 

  • Barbara I, Cremades J, Calvo S, Lopez-Rodriguez MC, Dosil J (2005) Check-list of the benthic marine and brackish Galician algae (NW Spain). An Jard Bot Madr 62:69–100

    Article  Google Scholar 

  • Bellorin AM, Oliveira MC, Oliveira EC (2004) Gracilaria vermiculophylla: a western Pacific species of Gracilariaceae (Rhodophyta) first recorded from the eastern Pacific. Phycol Res 52:69–79

    Article  Google Scholar 

  • Berke SK (2012) Biogeographic variability in ecosystem engineering: patterns in the abundance and behavior of the tube-building polychaete Diopatra cuprea. Mar Ecol Prog Ser 447:1–13

    Article  Google Scholar 

  • Bond DM, Finnegan EJ (2007) Passing the message on: inheritance of epigenetic traits. Trend Plant Sci 12:211–216

    Article  CAS  Google Scholar 

  • Bonsdorff E (1992) Drifting algae and zoobenthos—effects on settling and community structure. Neth J Sea Res 30:57–62

    Article  Google Scholar 

  • Byers JE, Gribben PE, Yeager C, Sotka EE (2012) Impacts of an abundant introduced ecosystem engineer within mudflats of the southeastern US coast. Biol Invasions 14:2587–2600

    Article  Google Scholar 

  • Cacabelos E, Engelen AH, Mejia A, Arenas F (2012) Comparison of the assemblage functioning of estuary systems dominated by the seagrass Nanozostera noltii versus the invasive drift seaweed Gracilaria vermiculophylla. J Sea Res 72:99–105

    Article  Google Scholar 

  • Chelaifa H, Mahe F, Ainouche M (2010) Transcriptome divergence between the hexaploid salt-marsh sister species Spartina maritima and Spartina alterniflora (Poaceae). Mol Ecol 19:2050–2063

    Article  PubMed  CAS  Google Scholar 

  • Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    Article  CAS  Google Scholar 

  • Crooks JA, Khim HS (1999) Architectural vs. biological effects of a habitat-altering, exotic mussel, Musculista senhousia. J Exp Mar Biol Ecol 240:53–75

    Google Scholar 

  • Cullis CA (2005) Mechanisms and control of rapid genomic changes inflax. Ann Bot (London) 95:201–206

    Article  CAS  Google Scholar 

  • De Carvalho JF, Poulain J, Silva CD, Wincker P, Michon-Coudouel S, Dheilly A, Naquin D, Boutte J, Salmon A, Ainouche M (2013) Transcriptome de novo assembly from next-generation sequencing and comparative analyses in the hexaploid salt marsh species Spartina maritima and Spartina alterniflora (Poaceae). Heredity 110:181–193

    Article  CAS  Google Scholar 

  • Farrell P, Fletcher RL (2006) An investigation of dispersal of the introduced brown alga Undaria pinnatifida (Harvey) Suringar and its competition with some species on the manmade structures of Torquay Marina (Devon, UK). J Exp Mar Biol Ecol 334:236–243

    Article  Google Scholar 

  • Freshwater DW, Montgomery F, Greene JK, Hamner RM, Williams M, Whitfield PE (2006) Distribution and identification of an invasive Gracilaria species that is hampering commercial fishing operations in southeastern North Carolina, USA. Biol Invasions 8:631–637

    Article  Google Scholar 

  • Guillemin ML, AitAkki S, Givernaud T, Mouradi A, Valeo M, Destombe C (2008) Molecular characterization and development of rapid molecular methods to identify species of Gracilariaceae from the Atlantic coast of Morocco. Aquat Bot 89:324–330

    Article  CAS  Google Scholar 

  • Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241

    Article  PubMed  Google Scholar 

  • Henikoff S (2005) Rapid changes in plant genomes. Plant Cell 17:2852–2855

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hewitt CL, Campbell ML, Schaffelke B (2007) Introduction of seaweeds: accidental transfer pathways and mechanisms. Bot Mar 50:326–337

    Article  Google Scholar 

  • Inderjit Chapman D, Ranelletti M, Kaushik S (2006) Invasive marine algae: an ecological perspective. Bot Rev 72:153–178

    Article  Google Scholar 

  • Jensen AT, Uldahl AG, Sjogren KP, Khan M (2007) The invasive macroalgae Gracilaria vermiculophylla—effects of salinity, nitrogen availability, irradiance and grazing on the growth rate. Master thesis, Department of Environmental, Social and Spatial Change, Roskilde University, Denmark

  • Johnston CA, Lipcius RN (2012) Exotic macroalga Gracilaria vermiculophylla provides superior nursery habitat for native blue crab in Chesapeake Bay. Mar Ecol Prog Ser 467:137–146

    Article  Google Scholar 

  • Kim JK, Kovtun K, Yarish C (2012) Tolerance to hypo-osmotic stress and low temperature determines the spread of non-indigenous Gracilaria vermiculophylla. J Phycol 48:S46

    Article  Google Scholar 

  • Kronvang B, Aertebjerg G, Grant R, Kristensen P, Hovmand M, Kirkegaard J (1993) Nationwide monitoring of nutrients and their ecological effects—state of the Danish aquatic environment. Ambio 22(4):176–187

    Google Scholar 

  • Lambert WJ, Levin PS, Berman J (1992) Changes in the structure of a New England (USA) kelp bed: the effects of an introduced species? Mar Ecol Prog Ser 88:303–307

    Article  Google Scholar 

  • Lawson SE, McGlathery KJ, Wiberg PL (2012) Enhancement of sediment suspension and nutrient flux by benthic macrophytes at low biomass. Mar Ecol Prog Ser 448:259–270

    Article  Google Scholar 

  • Lippson AJ, Lippson RL (1997) Life in the Chesapeake Bay. The John Hopkins University Press, Baltimore

    Google Scholar 

  • Lobban CS, Harrison PJ (1997) Seaweed ecology and physiology. Cambridge University Press, Cambridge

    Google Scholar 

  • Madsen JD, Chambers PA, James WF, Koch EW, Westlake DF (2001) The interaction between water movement, sediment dynamics and submersed macrophytes. Hydrobiologia 444:71–84

    Article  Google Scholar 

  • Martínez-Lüscher J, Holmer M (2010) Potential effects of the invasive species Gracilaria vermiculophylla on Zostera marina metabolism and survival. Mar Environ Res 69:345–349

    Article  PubMed  CAS  Google Scholar 

  • Meyercordt J, Gerbersdorf S, Meyer-Reil LA (1999) Significance of pelagic and benthic primary production in two shallow coastal lagoons of different degrees of eutrophication in the southern Baltic Sea. Aquat Microb Ecol 20(3):273–284

    Article  Google Scholar 

  • Nejrup LB, Pedersen MF (2012) The effect of temporal variability in salinity on the invasive red alga Gracilaria vermiculophylla. Eur J Phycol 47:254–263

    Article  Google Scholar 

  • Nettleton JC, Mathieson AC, Thornber C, Neefus CD, Yarish C (2013) Introductions of Gracilaria vermiculophylla (Rhodophyta, Gracilariales) to New England, USA: estimated arrival times and current distribution. Rhodora 115:28–41

    Article  Google Scholar 

  • Newton C, Bracken MES, McConville M, Rodrigue K, Thornber CS (2013a) Invasion of the red seaweed Heterosiphonia japonica spans biogeographic provinces in the western North Atlantic Ocean. PLoS ONE 8(4):e62661

    Article  CAS  Google Scholar 

  • Newton C, Guidone M, Thornber CS (2013b) Impacts of invasive Gracilaria vermiculophylla on the reproductive ecology of native benthic invertebrates. SICB Annual Meeting 2013, January 3–7, 2013, San Francisco, CA, USA

  • Nyberg CD (2007) Introduced marine macroalgae and habitat modifiers: the ecological role and significant attributes. Doctoral thesis, Department of Marine Ecology, Goteborg University, Goteborg, Sweden

  • Nyberg CD, Wallentinus I (2005) Can species traits be used to predict marine macroalgal introductions? Biol Invasions 7:265–279

    Article  Google Scholar 

  • Nyberg CD, Wallentinus I (2009) Long-term survival of an introduced red alga in adverse conditions. Mar Biol Res 5:304–308

    Article  Google Scholar 

  • Nyberg CD, Thomsen MS, Wallentinus I (2009) Flora and fauna associated with the introduced red alga Gracilaira vermiculophylla. Eur J Phycol 44:395–403

    Article  Google Scholar 

  • Nylund GM, Weinberger F, Rempt M, Pohnert G (2011) Metabolomic assessment of induced and activated chemical defence in the invasive red alga Gracilaria vermiculophylla. PLoS ONE 6(12):e29359

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ohmi H (1956) Contributions to the Knowledge of Gracilariaceae from Japan, II: on a new species of the genus Gracilariopsis, with some considerations on its ecology. Bull Fac Fish Hokkaido Univ 6:271–279

    Google Scholar 

  • Orth RJ, Olyarnik S, Short FT, Waycott M, Williams SL, Carruthers TJB, Dennison WC, Duarte CM, Fourquerean JW, Heck KL, Hughes RA, Kendrick GA, Kenworthy JW (2006) A global crisis for seagrass ecosystems. Bioscience 56(12):987–996

    Article  Google Scholar 

  • Pérez JE, Nirchio M, Alfonsi C, Munoz C (2006) The biology of invasions: the genetic adaptation paradox. Biol Invasions 8:1115–1121

    Article  Google Scholar 

  • Pinon-Gimate A, Serviere-Zaragoza E, Ochoa-Izaguirre MJ, Páez-Osuna F (2008) Species composition and seasonal changes in macroalgal blooms in lagoons along the southeastern Gulf of California. Bot Mar 51:112–123

    Article  Google Scholar 

  • Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294

    Article  PubMed  CAS  Google Scholar 

  • Prentis PJ, Woolfit M, Thomas-Hall SR, Ortiz-Barrientos D, Pavasovic A, Lowe AJ, Schenk PM (2010) Massive lyparallel sequencing and analysis of expressed sequence tags in a successful invasive plant. Ann Bot (London) 106:1009–1017

    Article  CAS  Google Scholar 

  • Raikar S, Iima M, Fujita Y (2001) Effect of temperature, salinity and light intensity on the growth of Gracilaria spp. (Gracilariales, Rhodophyta) from Japan, Malaysia and India. Indian J Mar Sci 30:98–104

    Google Scholar 

  • Rempt M, Weinberger F, Grosser K, Phnert G (2012) Conserved and species-specific oxylipin pathways in the wound-activated chemical defense of the noninvasive red alga Gracilaria chilensis and the invasive Gracilaria vermiculophylla. Beilstein J Org Chem 8:283–289

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Roleda MY, Nyberg CD, Wulff A (2012) UVR defense mechanisms in eurytopic and invasive Gracilaria vermiculophylla (Gracilariales, Rhodophyta). Physiol Plantarum 146:205–216

    Article  CAS  Google Scholar 

  • Rueness J (2005) Life histories and molecular sequences of Gracilaria vermiculophylla. Phycologia 44:120–128

    Article  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Ann Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Saunders GW (2009) Routine DNA barcoding of Canadian Gracilariales (Rhodophyta) reveals the invasive species Gracilaria vermiculophylla in British Columbia. Mol Ecol Res 9:141–150

    Article  CAS  Google Scholar 

  • Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae—a growing concern. J Appl Phycol 18:529–541

    Article  Google Scholar 

  • Schrey AW, Coon CAC, Grispo MT, Award M, Imboma T, McCoy ED, Mushinsky HR, Richard CL, Martin LB (2012) Epigenetic variation may compensate for decreased genetic variation with introductions: a case study using house sparrows (Passer domesticus) on two continents. Genet Res Int doi:10.1155/2012/979751

  • Sfriso A, Maistro S, Andreoli C, Moro I (2010) First record of Gracilaria vermiculophylla (Gracilariales, Rhodophyta) in the Po Delta Lagoons, Mediterranean Sea (Italy). J Phycol 46:1024–1027

    Article  Google Scholar 

  • Staehr PA, Pedersen MF, Thomsen MS, Wernberg T, Krause-Jensen D (2000) Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. Mar Ecol Prog Ser 207:79–88

    Article  Google Scholar 

  • Teso SV, Bigatti G, Casas GN, Piriz ML, Penchaszadeh PE (2009) Do native grazers from Patagonia, Argentina, consume the invasive kelp Undaria pinnatifida? Rev Mus Argentino Cienc Nat 11(1):7–14

    Google Scholar 

  • Thomsen MS (2010) Experimental evidence for positive effects of invasive seaweed on native invertebrates via habitat-formation in a seagrass bed. Aquat Invasions 5:341–346

    Article  Google Scholar 

  • Thomsen MS, McGlathery KJ (2005) Facilitation of macroalgae by the sedimentary tube forming polychaete Diopatra cuprea. Estuar Coast Shelf Sci 62:63–73

    Article  Google Scholar 

  • Thomsen MS, McGlathery KJ (2007) Stress tolerance of the invasive macroalgae Codium fragile and Gracilaria vermiculophylla in a soft-bottom turbid lagoon. Biol Invasions 9:499–513

    Article  Google Scholar 

  • Thomsen MS, Gurgel CFD, Fredericq S, McGlathery KJ (2005) Gracilaria vermiculophylla (Rhodophyta, Gracilariales) in Hog Island Bay, Virginia: a cryptic alien and invasive macroalga and taxonomic correction. J Phycol 42:139–141

    Article  Google Scholar 

  • Thomsen MS, Mcglathery KJ, Tyler AC (2006) Macroalgal distribution patterns in a shallow, soft-bottom lagoon, with emphasis on the non-native Gracilaria vermiculophylla and Codium fragile. Estuar Coast 29:465–473

    CAS  Google Scholar 

  • Thomsen MS, Stehr P, Nyberg CD, Krause-Jensen D, Schwaeter S, Silliman BR (2007) Gracilaria vermiculophylla in northern Europe, with focus on Denmark, and what to expect in the future. Aquat Invasions 3:1–12

    Google Scholar 

  • Thomsen MS, Wernberg T, Tuya F, Silliman BR (2009a) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Phycol 45(4):812–819

    Article  Google Scholar 

  • Thomsen MS, McGlathery KJ, Schartschild A, Silliman BR (2009b) Distribution and ecological role of the nonnative macroalga Gracilaria vermiculophylla in Virginia salt marshes. Biol Invasions 11:2303–2316

    Article  Google Scholar 

  • Tyler AC, McGlathery KJ (2006) Uptake and release of nitrogen by the macroalgae Gracilaria vermiculophylla (Rhodophyta). J Phycol 42:515–525

    Article  CAS  Google Scholar 

  • Tyler AC, McGlathery KJ, Macko SA (2005) Uptake of urea and amino acids by the macroalgae Ulva lactuca (Chlorophyta) and Gracilaria vermiculophylla (Rhodophyta). Mar Ecol Prog Ser 294:161–172

    Article  CAS  Google Scholar 

  • Weinberger F, Buchholz B, Karez R, Wahl M (2008) The invasive red alga Gracilaria vermiculophylla in the Baltic Sea: adaptation to brackish water may compensate for light limitation. Aquat Biol 3:251–264

    Article  Google Scholar 

  • Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Ann Rev Ecol Syst 38:327–359

    Article  Google Scholar 

  • Yokoya NS, Kakita H, Obika H, Kitamura T (1999) Effects of environmental factors and plant growth regulators on growth of the red alga Gracilaria vermiculophylla from Shikoku Island, Japan. Hydrobiologia 399:339–347

    Google Scholar 

  • Yoshida T, Yoshinaga K, Nkajima Y (1995) Check list of marine algae of Japan. Jpn J Phycol 43:115–171

    Google Scholar 

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Acknowledgments

We thank everyone who shared with us observations from both experimental and field surveys. We are grateful to two anonymous reviewers for their valuable and constructive comments on the original version of the manuscript. This work was supported by National Natural Science Foundation of China (No. 31000103) granted to Z. M. Hu, and by the US National Science Foundation Assembling the Tree of Life Program (DEB-1036495, DEB-0937978) granted to JMLB.

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Hu, ZM., Juan, LB. Adaptation mechanisms and ecological consequences of seaweed invasions: a review case of agarophyte Gracilaria vermiculophylla . Biol Invasions 16, 967–976 (2014). https://doi.org/10.1007/s10530-013-0558-0

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