Biological Invasions

, Volume 20, Issue 8, pp 1953–1959 | Cite as

Fragment quality and sediment organic loading regulate the survival of an invasive, clonal seaweed

  • Fabio Bulleri
  • Laura Tamburello
  • Antonio Pusceddu
  • Lisa Bonechi
  • Alessandro Cau
  • Davide Moccia
  • Paul E. Gribben
Invasion Note


Although propagule pressure is recognized as an important determinant of invasion dynamics, the role of propagule quality (i.e. the physical condition of a propagule) has received little attention. In particular, how the performance of vegetative propagules differing in quality varies across heterogeneous landscapes is yet to be explored. Caulerpa cylindracea is a clonal, invasive seaweed, widely distributed in the Mediterranean. By means of a laboratory experiment, we investigated how variation in the quality of seaweed fragments (intact vs. frond-removal vs. rhizoid-removal) influenced their survival on control versus sediments enriched with detritus from the native seagrass, Posidonia oceanica. The survival of seaweed fragments was low on non-enriched sediments, irrespective of their characteristics. On enriched sediments, survival was high in control and rhizoid-removal fragments, but low in frond-removal fragments. Our study shows that both fragment quality and sediment characteristics influence the survival of C. cylindracea propagules and, hence, long-term spreading dynamics of this seaweed. More generally, it brings novel evidence showing that the effects of propagule quality on invasion success are context-dependent.


Clonal plants Propagule quality Sediment organic loading Invasive macroalgae Caulerpa cylindracea 



We thank C. Ravaglioli for help with fieldworkd and two anonymous reviewers for providing comments on an earlier draft of the paper. AP was funded by the Fondazione di Sardegna (2016) and the Regione Autonoma della Sardegna (L7/2007), in the framework of the project Impact of Invasive Alien Species on Sardinian ecosystems. PEG was supported by an Australian Research Council Future Fellowships (FT140100322). LT was supported by the Italian Ministry for Education, University and Research (MIUR), under the call FIRB 2012, through the project HI-BEF (Unveiling hidden relationships between biodiversity and ecosystem functioning in Mediterranean rocky reefs) (protocol RBFR12RXWL), coordinated by C. Bonaviri (University of Palermo).

Supplementary material

10530_2018_1685_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 16 kb)


  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46Google Scholar
  2. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  3. Bulleri F, Benedetti-Cecchi L, Ceccherelli G, Tamburello L (2017) A few is enough: a low cover of a non-native seaweed reduces the resilience of Mediterranean macroalgal stands to disturbances of varying extent. Biol Invasions 19:2291–2305CrossRefGoogle Scholar
  4. Ceccherelli G, Cinelli F (1999) The role of vegetative fragmentation in dispersal of the invasive alga Caulerpa taxifolia in the Mediterranean. Mar Ecol Prog Ser 182:299–303CrossRefGoogle Scholar
  5. Ceccherelli G, Pinna S, Cusseddu V, Bulleri F (2014) The role of disturbance in promoting the spread of the invasive seaweed Caulerpa racemosa in seagrass meadows. Biol Invasions 16:2737–2745CrossRefGoogle Scholar
  6. Chisholm JRM, Moulin P (2003) Stimulation of nitrogen fixation in refractory organic sediments by Caulerpa taxifolia (Chlorophyta). Limnol Oceanogr 48:787–794CrossRefGoogle Scholar
  7. D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass fire cycle, and global change. Annu Rev Ecol Evol S 23:63–87CrossRefGoogle Scholar
  8. Estrada JA, Wilson CH, NeSmith JE, Flory SL (2016) Propagule quality mediates invasive plant establishment. Biol Invasions 18:2325–2332CrossRefGoogle Scholar
  9. Fraser MW, Statton J, Hovey RK, Laverock B, Hendrick GA (2016) Seagrass derived organic matter influences biogeochemistry, microbial communities, and seedling biomass partitioning in seagrass sediments. Plant Soil 400:133–146CrossRefGoogle Scholar
  10. Gennaro P, Piazzi L (2011) Synergism between two anthropic impacts: Caulerpa racemosa var. cylindracea invasion and seawater nutrient enrichment. Mar Ecol Prog Ser 427:59–70CrossRefGoogle Scholar
  11. Khou M, Paul NA, Wright JT, Steinberg PD (2007) Intrinsic factors influence the attachment of fragments of the green alga Caulerpa filiformis. J Exp Mar Biol Ecol 352:331–342CrossRefGoogle Scholar
  12. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204CrossRefPubMedGoogle Scholar
  13. Lange R, Marshall DJ (2016) Propagule size and dispersal costs mediate establishment success of an invasive species. Ecology 97:569–575CrossRefPubMedGoogle Scholar
  14. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228CrossRefPubMedGoogle Scholar
  15. Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology. Wiley, New YorkGoogle Scholar
  16. Mateo MA, Romero J (1997) Detritus dynamics in the seagrass Posidonia oceanica: elements for an ecosystem carbon and nutrient budget. Mar Ecol Prog Ser 151:43–53CrossRefGoogle Scholar
  17. Pacciardi L, De Biasi AM, Piazzi L (2011) Effects of Caulerpa racemosa invasion on soft-bottom assemblages in the Western Mediterranean Sea. Biol Invasions 13:2677–2690CrossRefGoogle Scholar
  18. Piazzi L, Balata D (2008) The spread of Caulerpa racemosa var. cylindracea in the Mediterranean Sea: an example of how biological invasions can influence beta diversity. Mar Environ Res 65:50–61CrossRefPubMedGoogle Scholar
  19. Piazzi L, Balata D (2009) Invasion of alien macroalgae in different Mediterranean habitats. Biol Invasions 11:193–204CrossRefGoogle Scholar
  20. Piazzi L, Meinesz A, Verlaque M et al (2005) Invasion of Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea: an assessment of the spread. Cryptogam Algol 26:189–202Google Scholar
  21. Piazzi L, Balata D, Bulleri F, Gennaro P, Ceccherelli G (2016) The invasion of Caulerpa cylindracea in the Mediterranean: the known, the unknown and the knowable. Mar Biol 163:161CrossRefGoogle Scholar
  22. Pusceddu A, Sarà G, Armeni M, Fabiano M, Mazzola A (1999) Seasonal and spatial changes in the sediment organic matter of a semi-enclosed marine system (W-Mediterranean Sea). Hydrobiologia 397:59–70CrossRefGoogle Scholar
  23. Pusceddu A, Fraschetti S, Scopa M, Rizzo L, Danovaro R (2016) Meiofauna communities, nematode diversity and C degradation rates in seagrass (Posidonia oceanica L.) and unvegetated sediments invaded by the algae Caulerpa cylindracea (Sonder). Mar Environ Res 119:88–99CrossRefPubMedGoogle Scholar
  24. Quinn LD, Holt JS (2009) Ecological correlates of invasion by Arundo donax in three southern California riparian habitats. Biol Invasions 10:591–601CrossRefGoogle Scholar
  25. Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661CrossRefGoogle Scholar
  26. Renoncourt L, Meinesz A (2002) Formation of propagules on an invasive strain of Caulerpa racemosa (Chlorophyta) in the Mediterranean Sea. Phycologia 41:533–535CrossRefGoogle Scholar
  27. Rizzo L, Pusceddu A, Stabili L, Alifano P, Fraschetti S (2017) Potential effects of an invasive seaweed (Caulerpa cylindracea, Sonder) on sedimentary organic matter and microbial metabolic activities. Sci Rep 7(1):12113CrossRefPubMedPubMedCentralGoogle Scholar
  28. Sandrini-Neto L, Camargo MG (2012) GAD: an R package for ANOVA designs from general principles. Available on CRANGoogle Scholar
  29. Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102CrossRefGoogle Scholar
  30. Smith CM, Walters MJ (1999) Fragmentation as a strategy for Caulerpa species: fates of fragments and implications for management of an invasive weed. Mar Ecol 20:307–319CrossRefGoogle Scholar
  31. Stabili L, Rizzo L, Pizzolante G, Alifano P, Fraschetti S (2017) Spatial distribution of the culturable bacterial community associated with the invasive alga Caulerpa cylindracea in the Mediterranean Sea. Marine Environ Res 125:90–98CrossRefGoogle Scholar
  32. Statton J, Cambridge ML, Dixon KW (2013) Aquaculture of Posidonia australis seedlings for seagrass restoration programs: effect of sediment type and organic enrichment on growth. Restor Ecol 21:250–259CrossRefGoogle Scholar
  33. Terlizzi A, Felline S, Lionetto MG, Caricato R, Perfetti V, Cutignano A, Mollo E (2011) Detrimental physiological effects of the invasive alga Caulerpa racemosa on the Mediterranean white seabream Diplodus sargus. Aquat Biol 12:109–117CrossRefGoogle Scholar
  34. Uyà M, Maggi E, Mori G, Nuccio C, Gribben P, Bulleri F (2017) Carry over effects of nutrient addition on the recovery of an invasive seaweed from the winter die-back. Mar Environ Res 126:37–44CrossRefPubMedGoogle Scholar
  35. Uyà M, Bulleri F, Gribben P (2018) Propagules are not all equal: traits of vegetative fragments and disturbance regulate invasion success. Ecology. PubMedGoogle Scholar
  36. Verlaque M, Afonso-Carrillo J, Candelaria Gil-Rodríguez M, Durand C, Boudouresque CF, Le Parco Y (2004) Blitzkrieg in a marine invasion: Caulerpa racemosa var. cylindracea (Bryopsidales, Chlorophyta) reaches the Canary Islands (North-East Atlantic). Biol Invasions 6:269–281CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Dipartimento di BiologiaUniversità di Pisa, CoNISMaPisaItaly
  2. 2.Dipartimento di Scienze della Vita e dell’AmbienteUniversità degli Studi di CagliariCagliariItaly
  3. 3.Dipartimento di Architettura, Design e UrbanisticaUniversità di SassariSassariItaly
  4. 4.Centre for Marine Bio-Innovation, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  5. 5.Sydney Institute of Marine ScienceMosmanAustralia

Personalised recommendations