Skip to main content

Advertisement

Log in

Impact of an invasive alga (Womersleyella setacea) on sponge assemblages: compromising the viability of future populations

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

Abstract

The effects of invasive species on native fauna are understudied, even though their consequences should be taken into consideration for the proper conservation and management of marine systems. Furthermore, bioinvasions may have greater consequences if they affect key structural species with slow dynamics such as marine sponges. We propose that reproductive output could be used as a potential early warning signal to detect possible future changes in population trends of long-lived species (i.e. sponges) as a result of biological invasions. The aim of this study was to investigate the effects of invasive algal (Womersleyella setacea) overgrowth on sponge reproduction by comparing the presence of reproductive elements (spermatic cysts, oocytes, embryos, and larvae) in sponges covered by a thick carpet of the invasive algae and in sponges dwelling in the same habitat but without the invasive algae. Three variables were calculated to assess the impact of the invasive alga on sponge reproduction: the reproductive effort, the proportion of individuals in reproduction, and the size of the reproductive structures. We studied eight sponge species representing the main components of the deep rocky reefs of the area. Our results showed that W. setacea had a strong negative effect on sponge reproduction in six out of eight sponge species studied, with lower and even nil reproductive structures on the sponges subjected to the algal overgrowth. Thus, considering that sexual reproduction is necessary for the persistence of most sponge populations, a significant and constant reduction of the reproductive effort may compromise their viability and affect future trends in these benthic systems.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams SM, Shepard KL, Greeley MS, Jimenez BD Jr, Ryon MG et al (1989) The use of bioindicators for assessing the effects of pollutant stress on fish. Mar Environ Res 28:459–464

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Airoldi L, Rindi F, Piazzi L, Cinelli F (1995) Distribution of Polysiphonia setacea (Rhodomelaceae, Rhodophyta) Hollenberg in the Mediterranean and possible means of diffusion. Biol Mar Med 2:343–344

    Google Scholar 

  • Athanasiadis A (1997) North Aegean marine algae. Womersleyella setacea (Hollenberg) R.E. Norris (Rhodophyta, Ceramiales). Bot Mar 40:473–476

  • Baldacconi R, Corriero G (2009) Effects of the spread of the alga Caulerpa racemosa var. cylindracea on the sponge assemblage from coralligenous concretions of the Apulian coast (Ionian Sea, Italy). Mar Ecol 30:337–345

    Article  Google Scholar 

  • Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195

    Google Scholar 

  • Becerro MA, Uriz MJ, Turon X (1994) Trends in space occupation by the encrusting sponge Crambe crambe: variation in shape as a function of size and environment. Mar Biol 121:301–307

    Article  Google Scholar 

  • Bensoussan N, Romano JC, Harmelin JG, Garrabou J (2010) High resolution characterization of northwest Mediterranean coastal waters thermal regimes: to better understand responses of benthic communities to climate change. Estuar Coast Shelf Sci 87:431–441

    Article  Google Scholar 

  • Blanquer A, Uriz MJ (2010) Population genetics at three spatial scales of a rare sponge living in fragmented habitats. BMC Evol Biol 10:13. doi:10.1186/1471-2148-10-13

    Article  PubMed  Google Scholar 

  • Boudouresque CF (2004) Marine biodiversity in the Mediterranean: status of species, populations and communities. Sci Rep Port-Cros Natl Park 20:97–146

    Google Scholar 

  • Boudouresque CF, Verlaque M (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Pollut Bull 44:32–38

    Article  PubMed  CAS  Google Scholar 

  • Britton-Simmons KH (2004) Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington State, USA. Mar Ecol Prog Ser 277:61–78

    Article  Google Scholar 

  • Bruno JF, Fridley JD, Bromberg KD, Bertness MD (2005) Insights into biotic interactions from studies of species invasions. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates, Inc., Sunderland, pp 14–40

    Google Scholar 

  • Carballo JL, Naranjo S, García-Gómez JC (1996) Use of marine sponges as stress indicators in marine ecosystem at Algeciras Bay (southern Iberian Peninsula). Mar Ecol Prog Ser 135:109–122

    Article  Google Scholar 

  • Casas-Güell E, Teixidó N, Cebrián E, Garrabou J (2012) Community structure and biodiversity patterns in coralligenous outcrops over spatial and temporal scales. Global Questions on advanced biology. Barcelona (Spain)

  • Cebrian E, Uriz MJ, Martí R, Turon X (2003) Sublethal effects of contamination on the Mediterranean sponge Crambe crambe: copper accumulation and biological responses. Mar Pollut Bull 46:1273–1284

    Article  PubMed  CAS  Google Scholar 

  • Cebrian E, Martí R, Agell G, Uriz MJ (2006) Response to heavy metal pollution of the Mediterranean sponge Chondrosia reniformis Nardo. Environ Pollut 141:452–458

    Article  PubMed  CAS  Google Scholar 

  • Cebrian E, Uriz MJ, Turon X (2007) Sponges as bioaccumulators of heavy metals: spatial and temporal variations. Environ Toxicol Chem 26:2430–2439

    Article  PubMed  CAS  Google Scholar 

  • Cebrian E, Uriz MJ, Garrabou J, Ballesteros E (2011) Sponge mass mortalities in a warming Mediterranean sea: are cyanobacteria-harboring species worse off? PLoS ONE 6(6):e20211. doi:10.1371/journal.pone.0020211

    Article  PubMed  CAS  Google Scholar 

  • Cebrian E, Linares C, Marschall C, Garrabou J (2012) Exploring the effects of invasive algae on the persistence of gorgonian populations enduring climate-induced mortalities. Biol Invasions 14:2647–2656

    Article  Google Scholar 

  • Cerrano C, Bavestrello G, Bianchi N (2000) A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (NW Mediterranean), summer 1999. Ecol Lett 3:284–293

    Article  Google Scholar 

  • Coma R, Pola E, Ribes M, Zabala M (2004) Long-term assessment of the patterns of mortality of a temperate octocoral in protected and unprotected areas: a contribution to conservation and management needs. Ecol Appl 14:1466–1478

    Article  Google Scholar 

  • Davis AR, Roberts DE, Cummins SP (1997) Rapid invasion of a sponge-dominated deep-reef by Caulerpa scalpelliformis (Chlorophyta) in Botany Bay, New South Wales. Aust J Ecol 22:146–150

    Article  Google Scholar 

  • De Caralt S, Otjens H, Uriz MJ, Wijffels RH (2007) Cultivation of sponge larvae: settlement, survival and growth of juveniles. Mar Biotechnol 9:592–605

    Article  PubMed  CAS  Google Scholar 

  • Fromont J, Bergquist PR (1994) Reproductive biology of three sponge species of the genus Xestospongia (Porifera: Demospongiae: Petrosida) from the Great Barrier Reef. Coral Reefs 13:119–126

    Article  Google Scholar 

  • Garrabou J, Harmelin JG (2002) A 20-year study on life-history traits of a harvested long-lived temperate coral in the NW Mediterranean: insights into conservation and management needs. J Anim Ecol 71:966–978

    Article  Google Scholar 

  • Garrabou J, Perez T, Sartoretto S, Harmelin JG (2001) Mass mortality event in red coral (Corallium rubrum, Cnidaria, Anthozoa, Octocorallia) populations in Provence region (France, NW Mediterranean). Mar Ecol Prog Ser 217:263–272

    Article  Google Scholar 

  • Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27

    Article  Google Scholar 

  • Linares C, Cebrian E, Coma R (2012) Effects of turf algae on recruitment and juvenile survival of gorgonian corals. Mar Ecol Prog Ser 452:81–88

    Article  Google Scholar 

  • Maldonado M, Riesgo A (2009) Gametogenesis, embryogenesis, and larval features of the oviparous sponge Petrosia ficiformis (Haplosclerida, Demospongiae). Mar Biol 156:2181–2197

    Article  Google Scholar 

  • Mariani S, Uriz MJ, Turon X (2005) The dynamics of sponge larvae assemblages from northwestern Mediterranean nearshore bottoms. J Plankton Res 27:249–262

    Article  Google Scholar 

  • Olden JD, Poff NL (2004) Ecological process driving biotic homogenization: testing a mechanistic model using fish faunas. Ecology 85:1867–1875

    Article  Google Scholar 

  • Perez T, Garrabou J, Sartoretto S, Harmelin JG, Francour P et al (2000) Mortalité massive d’invertébrés marins: Un événement sans précédent en Méditerranée nord-occidentale. CR Acad Sci Paris 323:853–865

    Article  CAS  Google Scholar 

  • Perez T, Vacelet J, Rebouillon P (2004) In situ comparative study of several Mediterranean sponges as potential biomonitors of heavy metals. In: Pansini M, Pronzato R, Bavestrello G, Manconi R (eds) Sponge science in the new millennium. Genova, Officine Grafiche Canessa Rapallo, pp 517–525

    Google Scholar 

  • Pérez-Porro A-R, González J, Uriz MJ (2012) Reproductive traits explain contrasting ecological features in sponges: the sympatric poecilosclerids Hemimycale columella and Crella elegans as examples. Hydrobiologia 687:315–330

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Piazzi L, Balata D, Ceccherelli G, Cinelli F (2005) Interactive effect of sedimentation and Caulerpa racemosa var. cylindracea invasion on macroalgal assemblages in the Mediterranean Sea. Estuar Coast Shelf Sci 64:467–474

    Article  Google Scholar 

  • Pimentel D, Lach L, Zuñiga R, Morrison D (2000) Environmental and economic costs associated to non-indigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • Pronzato R (1999) Sponge-fishing, disease and farming in the Mediterranean Sea. Aquat Conserv 9:485–493

    Article  Google Scholar 

  • Reiswig HM (1971) Particle feeding in natural populations of three marine demosponges. Biol Bull 141:568–591

    Article  Google Scholar 

  • Ribes M, Coma R, Atkinson MJ, Kinzie RA (2005) Sponges and ascidians control removal of particulate organic nitrogen from coral reef water. Limnol Oceanogr 50:1480–1489

    Article  CAS  Google Scholar 

  • Rodriguez- Prieto C, Joher S, Cebrian E (2010) Light and temperature requirements for survival and growth of Mediterranean Womersleyella setacea. In: Proceedings of the IV Medical Symposium Mar Vegetation 111–115

  • Rützler K (1970) Spatial competition among Porifera: solution by epizoism. Oecologia 5:85–95

    Article  Google Scholar 

  • Schaffelke B, Hewitt CL (2007) Impacts of introduced seaweeds. Bot Mar 50:397–417

    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 

  • Simpson TL (1984) The cell biology of songes. Springer, New York, pp 517–523

    Book  Google Scholar 

  • Streftaris N, Zenetos A (2006) Alien Marine Species in the Mediterranean—the 100 ‘Worst Invasives’ and their Impact. Med Mar Sci 7:87–118

    Google Scholar 

  • Teixidó N, Garrabou J, Harmelin JG (2011) Low dynamics, high longevity and persistence of sessile structural species dwelling on Mediterranean coralligenous outcrops. PLoS ONE 6(8):e23744. doi:10.1371/journal.pone.0023744

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Uriz MJ, Rosell D, Martin D (1992) The sponge population of the Cabrera archipelago (Balearic Islands): characteristics, distribution and abundance of the most representative species. PSZNI Mar Ecol 113:101–117

    Article  Google Scholar 

  • Uriz MJ, Turon X, Becerro MA, Galera J, Lozano J (1995) Patterns of resource allocation to somatic, defensive, and reproductive functions in the Mediterranean encrusting sponge Crambe crambe (Demospongiae, Poecilosclerida). Mar Ecol Prog Ser 124:159–170

    Article  Google Scholar 

  • Uriz MJ, Becerro MA, Tur JM, Turon X (1996) Location of toxicity within the Mediterranean sponge Crambe crambe (Demospongiae: Poecilosclerida). Mar Biol 124:583–590

    Article  CAS  Google Scholar 

  • Uriz MJ, Maldonado M, Turon X, Marti R (1998) How do reproductive output, larval behaviour, and recruitment contribute to adult spatial patterns in Mediterranean encrusting sponges? Mar Ecol Prog Ser 167:137–148

    Article  Google Scholar 

  • Vacelet J (1979) La place des spongiaires dans les systemes trophiques marins. In: Lévi C, Boury-Esnault N (eds) Biologie des Spongiaires. Editions du CRNS, Paris, pp 259–270

    Google Scholar 

  • Verdenal B, Diana C, Arnoux A, Vacelet J (1990) Pollutant levels in Mediterranean commercial sponges. In: Rützler K (ed) New perspectives in sponge biology. Smithsonian Institution Press, Washington, pp 516–524

    Google Scholar 

  • Verlaque M (1994) Inventaire des plantes introduites en Méditerranée: origines et répercussions sur l’environnement et les activités humaines. Oceanol Acta 17:1–23

    Google Scholar 

  • Whalan S, Battershill C, de Nys R (2007) Variability in reproductive output across a water quality gradient for a tropical marine sponge. Mar Biol 153:163–169

    Article  Google Scholar 

  • Wulff J (2006) Rapid diversity and abundance decline in a Caribbean coral reef sponge community. Biol Conserv 127:167–176

    Article  Google Scholar 

  • Zuljevic A, Thibaut T, Despalatovic M, Cottalorda JM, Nikolic V et al (2011) Invasive alga Caulerpa racemosa var. cylindracea makes a strong impact on the Mediterranean sponge Sarcotragus spinosulus. Biol Invasions 13:2303–2308

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank J. González for her help in the sample processing at the laboratory and to all the staff of the Scandola Natural Reserve for permissions and facilities during the sampling. Financial support was provided by an EU reintegration grant (ERG-2009-248252) and the project Tracking Changes in the Marine benthos by Novel Molecular Tools: Individuals, populations, communities (BENTHOMICS) from the Ministerio de Ciencia e Innovación of the Spanish Government (MICINN) (CTM2010-22218-C02). SC and EC were funded by a Juan de la Cierva Postdoctoral Fellowship. EC is part of the Marine Conservation Research Group (www.medrecover.org) of the Autonomous Government of Catalonia. The funding organizations had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sonia de Caralt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Caralt, S., Cebrian, E. Impact of an invasive alga (Womersleyella setacea) on sponge assemblages: compromising the viability of future populations. Biol Invasions 15, 1591–1600 (2013). https://doi.org/10.1007/s10530-012-0394-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-012-0394-7

Keywords

Navigation