Skip to main content

Advertisement

SpringerLink
Log in

The role of disturbance in promoting the spread of the invasive seaweed Caulerpa racemosa in seagrass meadows

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Human disturbances, such as anchoring and dredging, can cause physical removal of seagrass rhizomes and shoots, leading to the fragmentation of meadows. The introduced green alga, Caulerpa racemosa, is widely spread in the North-West Mediterranean and, although it can establish in both degraded and pristine environments, its ability to become a dominant component of macroalgal assemblages seems greater in the former. The aim of this study was to estimate whether the spread of C. racemosa depends on the intensity of disturbance to the canopy structure of Posidonia oceanica. A field experiment was started in July 2010 when habitat complexity of a P. oceanica meadow was manipulated to simulate mechanical disturbances of different intensity: rhizome damage (High disturbance intensity = H), leaf removal (Low disturbance intensity = L), and undisturbed (Control = C). Disturbance was applied within plots of different size (40 × 40 cm and 80 × 80 cm), both inside and at the edge of the P. oceanica meadow, according to an orthogonal multifactorial design. In November 2011 (16 months after the start of the experiment), no C. racemosa was found inside the seagrass meadow, while, at the edge, the cover of the seaweed was dependent on disturbance intensity, being greater where the rhizomes had been damaged (H) than in leaf removal (L) or undisturbed (C) plots. The results of this study indicate that physical disturbance at the margin of seagrass meadows can promote the spread of C. racemosa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Airoldi L (1998) Roles of disturbance, sediment stress, and substratum retention on spatial dominance in algal turf. Ecology 79:2759–2770

    Article  Google Scholar 

  • Ardizzone G, Belluscio A, Maiorano L (2006) Long-term change in the structure of a Posidonia oceanica landscape and its reference for a monitoring plan. Mar Ecol 27:299–309

    Article  Google Scholar 

  • Boudouresque CF (2003) The erosion of Mediterranean biodiversity. In: Rodriguez-Prieto C, Pardini G (eds) The Mediterranean sea: an overview of its present state and plans for future protection. Servei de Publicacions de la Universitat de Girona, Girona, pp 53–112

    Google Scholar 

  • Boudouresque CF, Ballesteros E, Ben Maiz N, Boisset F, Bouladier E, Cinelli F, Cirik S, Cormaci M, Jeudy De Grissac A, Laborel J, Lanfranco E, Lundberg B, Mayhoub H, Meisnez A, Panayotidis P, Semroud R, Sinnassamy JM, Span A, Vuignier G (1990) Livre rouge “Gérard Vuigner” des végétaux, peuplements et paysages marins menaces de Méditerranée. PNUE Publications, Athens 250

    Google Scholar 

  • Boudouresque CF, Bernard G, Pergent G, Shili A, Verlaque M (2009) Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review. Bot Mar 52(5):395–418

    Article  Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:19–125

    Article  Google Scholar 

  • Bulleri F, Balata D, Bertocci I, Tamburello L, Benedetti-Cecchi L (2010) The seaweed Caulerpa racemosa on Mediterranean rocky reefs: from passenger to driver of ecological change. Ecology 91:2205–2212

    Article  PubMed  Google Scholar 

  • Bulleri F, Alestra T, Ceccherelli G, Tamburello L, Pinna S, Sechi N, Benedetti-Cecchi L (2011) Determinants of Caulerpa racemosa distribution in the north-western Mediterranean. Mar Ecol Prog Ser 431:55–67

    Article  Google Scholar 

  • Byers JE (2002) Physical habitat attribute mediates biotic resistance to non-indigenous species invasion. Oecologia 130:146–156

    Google Scholar 

  • Ceccherelli G, Piazzi L (2001) Dispersal of Caulerpa racemosa fragments in the Mediterranean: lack of detachment time effect on establishment. Bot Mar 44:209–213

    Article  Google Scholar 

  • Ceccherelli G, Piazzi L, Cinelli F (2000) Response of the non-indigenous Caulerpa racemosa (Forsskal) J-Agardh to the native seagrass Posidonia oceanica (L.) Delile: effect of density of shoots and orientation of edges of meadows. J Exp Mar Biol Ecol 243:227–240

    Article  Google Scholar 

  • Ceccherelli G, Piazzi L, Balata D (2002) Spread of introduced Caulerpa species in macroalgal habitats. J Exp Mar Biol Ecol 280:1–11

    Article  Google Scholar 

  • Ceccherelli G, Campo D, Milazzo M (2007) Short-term response of the slow growing seagrass Posidonia oceanica to simulated anchor impact. Mar Environ Res 63:341–349

    Article  CAS  PubMed  Google Scholar 

  • Clark GF, Johnston EL (2011) Temporal change in the diversity–invasibility relationship in the presence of a disturbance regime. Ecol Lett 14:52–57

    Article  PubMed  Google Scholar 

  • D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass: fire cycle, and global change. Ann Rev Ecol Evol S 23:63–87

    Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:524–534

    Article  Google Scholar 

  • Dayton PK (1975) Experimental evaluation of ecological dominance in a rocky intertidal community. Ecol Monogr 45:137–159

    Article  Google Scholar 

  • Dethier MN, Graham ES, Cohen S, Tear LM (1993) Visual versus random-point percent cover estimations: ‘objective’ is not always better. Mar Ecol Progr Ser 110:9–18

    Google Scholar 

  • Dietz H, Edwards PJ (2006) Recognition that causal processes change during plant invasion helps explain conflicts in evidence. Ecology 87:1359–1367

  • Driscoll DA (2007) How to find a metapopulation. Can J Zool 85:1031–1048

    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(2):343–352

  • Francour P, Ganteaume A, Poulain M (1999) Effect of boat anchoring in Posidonia oceanica seagrass beds in the Port-Cros national park (north-western Mediterranean sea). Aquat Conserv 9:391–400

    Article  Google Scholar 

  • Glasby TM (2013) Caulerpa taxifolia in seagrass meadows: killer or opportunistic weed? Biol Invas 15:1017–1035

    Article  Google Scholar 

  • Hemminga MA, Duarte CM (2000) Seagrass ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hobbs RT, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337

    Article  Google Scholar 

  • Irving AD, Connell SD (2006) Predicting understorey structure from the presence and composition of canopies: an assembly rule for marine algae. Oecologia 148:491–502

    Article  PubMed  Google Scholar 

  • Johnston EL, Keough MJ (2002) Direct and indirect effects of repeated pollution events on marine hard-substrate assemblages. Ecol Appl 12:1212–1228

    Google Scholar 

  • Katsanevakis S, Issaris Y, Poursanidis D, Thessalou-Legaki M (2010) Vulnerability of marine habitats to the invasive green alga Caulerpa racemosa var. cylindracea within a marine protected area. Mar Env Res 70:210–218

    Article  CAS  Google Scholar 

  • Kiparissis S, Fakiris E, Papatheodorou G, Geraga M, Kornaros M, Kapareliotis A, Ferentinos G (2011) Illegal trawling and induced invasive algal spread as collaborative factors in a Posidonia oceanica meadow degradation. Biol Invas 13:669–678

    Article  Google Scholar 

  • Klein J, Verlaque M (2008) The Caulerpa racemosa invasion: a critical review. Mar Poll Bull 56:645–650

    Article  Google Scholar 

  • Lohrer AM, Chiaroni LD, Hewitt JE, Thrush SF (2008) Biogenic disturbance determines invasion success in a subtidal soft-sediment system. Ecology 89:1299–1307

    Article  PubMed  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Milazzo M, Badalamenti F, Ceccherelli G, Chemello R (2004) Boat anchoring on Posidonia oceanica beds in a marine protected area (Italy, western Mediterranean): effect of anchor types in different anchoring stages. J Exp Mar Biol Ecol 299:51–62

    Article  Google Scholar 

  • Montefalcone M, Morri C, Peirano A, Albertelli G, Bianchi CN (2007) Substitution and phase shift within the Posidonia oceanica seagrass meadows of NW Mediterranean Sea. Estuar Coast Shelf Sci 75:63–71

    Article  Google Scholar 

  • Montefalcone M, Chiantore M, Lanzone A, Morri C, Albertelli G, Bianchi CN (2008) BACI design reveals the decline of the seagrass Posidonia oceanica induced by anchoring. Mar Poll Bull 56(9):1637–1645

    Article  CAS  Google Scholar 

  • Montefalcone M, Albertelli G, Morri C, Bianchi CN (2010) Patterns of wide-scale substitution within meadows of the seagrass Posidonia oceanica in NW Mediterranean Sea: invaders are stronger than natives. Aquat Conserv 20(5):507–515

    Article  Google Scholar 

  • Paine RT (2002) Trophic control of production in a rocky intertidal community. Science 296:736–739

    Article  CAS  PubMed  Google Scholar 

  • Pearson SM (1993) The spatial extent and relative influence of landscape-level factors on wintering bird populations. Landsc Ecol 8:3–18

    Article  Google Scholar 

  • Peirano A, Bianchi CN (1997) Decline of the seagrass Posidonia oceanica in response to environmental disturbance: a simulation-like approach off Liguria (NW Mediterranean Sea). In: Hawkins LE, Hutchinson S (eds) The response of Marine organisms to their environments. University of Southampton, UK, pp 87–95

    Google Scholar 

  • Pérès JM (1984) La regression des herbiers à Posidonia oceanica. In: Boudouresque CF, Jeudy De Grissac A, Olivier J (eds) First international workshop on Posidonia oceanica beds. GIS Posidonie Publ, France, pp 445–454

    Google Scholar 

  • Pergent G (1992) Key species in the Mediterranean littoral. The importance of Posidonia oceanica meadows. The European coastline study. European Science Foundation and Commission of the European Communities, Galway, pp 32–36

  • Pergent G, Pergent-Martini C, Boudouresque CF (1995) Utilisation de l’herbier à Posidonia oceanica comme indicateur biologique de la qualité du milieu littoral en Méditerranée: Etat des connaissances. Mésogée 54:3–29

    Google Scholar 

  • Piazzi L, Balata D (2009) Invasion of alien macroalgae in different Mediterranean habitats. Biol Inv 11:193–204

    Article  Google Scholar 

  • Piazzi L, Cinelli F (1999) Development and seasonal dynamics of a population of the tropical alga Caulerparacemosa (Forsskål) J Agardh in the Mediterranean. Cryptogam Algol 20:295–300

  • Piazzi L, Ceccherelli G, Cinelli F (2001) Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar Ecol Progr Ser 210:149–159

  • Piazzi L, Ceccherelli G, Balata D, Cinelli F (2003) Early patterns of Caulerpa racemosa in the Mediterranean Sea: the influence of algal turfs. J Mar Biol Assoc UK 83:27–29

    Google Scholar 

  • Piazzi L, Meinesz A, Verlaque M, Akçali B, Antolić B, Argyrou M, Balata D, Ballesteros E, Calvo S, Cinelli F, Cirik S, Cossu A, D’Archino R, Djellouli AS, Javel J, Lanfranco E, Mifsud C, Pala D, Panayotidis P, Peirano A, Pergent G, Petrocelli A, Ruitton S, Žuljević A, Ceccherelli G (2005) Invasion of Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea: an assessment of the spread. Cryptogam Algol 26:189–202

    Google Scholar 

  • Predick KI, Turner MG (2008) Landscape configuration and flood frequency influence invasive shrubs in floodplain forests of the Wisconsin River (USA). J Ecol 96:91–102

    Google Scholar 

  • Richardson DM, Holmes TM, Esler KJ, Galatowitsch SM et al (2000) Riparian vegetation degradation, alien plant invasions, and restoration prospects. Divers Distrib 13:126–139

    Article  Google Scholar 

  • Ricketts TH (2001) The matrix matters: effective isolation in fragmented landscapes. Am Nat 158:87–99

    Article  CAS  PubMed  Google Scholar 

  • Ruitton S, Javel F, Culioli JM, Meinesz A, Pergent G, Verlaque M (2005) First assessment of the Caulerpa racemosa (Caulerpales, Chlorophyta) invasion along the French Mediterranean coast. Mar Pollut Bull 50:1061–1068

    Article  CAS  PubMed  Google Scholar 

  • Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176

    Article  Google Scholar 

  • Tamburello L, Benedetti-Cecchi L, Ghedini G, Alestra T, Bulleri F (2012) Variation in the structure of subtidal landscapes in the NW Mediterranean Sea. Mar Ecol Progr Ser 457:29–41

    Article  Google Scholar 

  • Tamburello L, Bulleri F, Balata D, Benedetti-Cecchi L (2014) The role of overgrazing and anthropogenic disturbance in shaping spatial patterns of distribution of an invasive seaweed. J Appl Ecol. doi:10.1111/1365-2664.12199

  • Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273

    Article  PubMed  Google Scholar 

  • Thomas JA, Bourn NAD, Clarke RT, Stewart KE, Simcox DJ, Pearman GS, Curtis R, Goodger B (2001) The quality and isolation of habitat patches both determine where butterflies persist in fragmented landscapes. Proc R Soc Lond Ser B Biol Sci 268:1791–1796

    Article  CAS  Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge

    Google Scholar 

  • Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Forqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. P Natl Acad Sci USA 106(30):12377–12381

    Article  CAS  Google Scholar 

  • Wiens JA, Stenseth NC, Van Horne B, Ims RA (1993) Ecological mechanisms and landscape ecology. Oikos 66:369–380

    Article  Google Scholar 

  • Williams SL (2007) Introduced species in seagrass ecosystems: status and concerns. J Exp Mar Biol Ecol 350:89–110

    Article  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgments

We sincerely thank Francesco Mura for help with fieldwork and boating operations. S.P. was supported by funds from a “Regione Autonoma della Sardegna” (PO Sardegna FSE 2007-2013 LR7/2007) Grant. Two anonymous reviewers provided comments and constructive criticism on earlier draft.

Author information

Authors and Affiliations

  1. Dipartimento di Scienze della Natura e del Territorio, Polo Bionaturalistico, University of Sassari, Via Piandanna 4, 07100, Sassari, Italy

    Giulia Ceccherelli, Stefania Pinna & Valentina Cusseddu

  2. Dipartimento di Biologia, University of Pisa, Via Derna 1, 56126, Pisa, Italy

    Fabio Bulleri

Authors
  1. Giulia Ceccherelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefania Pinna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valentina Cusseddu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabio Bulleri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giulia Ceccherelli.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ceccherelli, G., Pinna, S., Cusseddu, V. et al. The role of disturbance in promoting the spread of the invasive seaweed Caulerpa racemosa in seagrass meadows. Biol Invasions 16, 2737–2745 (2014). https://doi.org/10.1007/s10530-014-0700-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-014-0700-7

Keywords

Search

Navigation