Biological Invasions

, Volume 15, Issue 7, pp 1591–1600 | Cite as

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

Original Paper

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.

Keywords

Invasive species Sponges Reproduction Mediterranean 

References

  1. 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 28:459–464CrossRefGoogle Scholar
  2. Airoldi L (1998) Roles of disturbance, sediment stress, and substratum retention on spatial dominance in algal turf. Ecology 79:2759–2770CrossRefGoogle Scholar
  3. 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 2:343–344Google Scholar
  4. Athanasiadis A (1997) North Aegean marine algae. Womersleyella setacea (Hollenberg) R.E. Norris (Rhodophyta, Ceramiales). Bot Mar 40:473–476Google Scholar
  5. 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 30:337–345CrossRefGoogle Scholar
  6. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195Google Scholar
  7. 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 121:301–307CrossRefGoogle Scholar
  8. 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 87:431–441CrossRefGoogle Scholar
  9. 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 PubMedCrossRefGoogle Scholar
  10. Boudouresque CF (2004) Marine biodiversity in the Mediterranean: status of species, populations and communities. Sci Rep Port-Cros Natl Park 20:97–146Google Scholar
  11. Boudouresque CF, Verlaque M (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Pollut Bull 44:32–38PubMedCrossRefGoogle Scholar
  12. 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 277:61–78CrossRefGoogle Scholar
  13. 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 14–40Google Scholar
  14. 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 135:109–122CrossRefGoogle Scholar
  15. 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)Google Scholar
  16. 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 46:1273–1284PubMedCrossRefGoogle Scholar
  17. Cebrian E, Martí R, Agell G, Uriz MJ (2006) Response to heavy metal pollution of the Mediterranean sponge Chondrosia reniformis Nardo. Environ Pollut 141:452–458PubMedCrossRefGoogle Scholar
  18. Cebrian E, Uriz MJ, Turon X (2007) Sponges as bioaccumulators of heavy metals: spatial and temporal variations. Environ Toxicol Chem 26:2430–2439PubMedCrossRefGoogle Scholar
  19. 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 PubMedCrossRefGoogle Scholar
  20. 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 14:2647–2656CrossRefGoogle Scholar
  21. 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 3:284–293CrossRefGoogle Scholar
  22. 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 14:1466–1478CrossRefGoogle Scholar
  23. 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 22:146–150CrossRefGoogle Scholar
  24. De Caralt S, Otjens H, Uriz MJ, Wijffels RH (2007) Cultivation of sponge larvae: settlement, survival and growth of juveniles. Mar Biotechnol 9:592–605PubMedCrossRefGoogle Scholar
  25. 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 13:119–126CrossRefGoogle Scholar
  26. 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 71:966–978CrossRefGoogle Scholar
  27. 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 217:263–272CrossRefGoogle Scholar
  28. Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27CrossRefGoogle Scholar
  29. Linares C, Cebrian E, Coma R (2012) Effects of turf algae on recruitment and juvenile survival of gorgonian corals. Mar Ecol Prog Ser 452:81–88CrossRefGoogle Scholar
  30. Maldonado M, Riesgo A (2009) Gametogenesis, embryogenesis, and larval features of the oviparous sponge Petrosia ficiformis (Haplosclerida, Demospongiae). Mar Biol 156:2181–2197CrossRefGoogle Scholar
  31. Mariani S, Uriz MJ, Turon X (2005) The dynamics of sponge larvae assemblages from northwestern Mediterranean nearshore bottoms. J Plankton Res 27:249–262CrossRefGoogle Scholar
  32. Olden JD, Poff NL (2004) Ecological process driving biotic homogenization: testing a mechanistic model using fish faunas. Ecology 85:1867–1875CrossRefGoogle Scholar
  33. 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 323:853–865CrossRefGoogle Scholar
  34. 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 517–525Google Scholar
  35. 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 687:315–330CrossRefGoogle Scholar
  36. Piazzi L, Balata D (2009) Invasion of alien macroalgae in different Mediterranean habitats. Biol Invasions 11:193–204CrossRefGoogle Scholar
  37. 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 64:467–474CrossRefGoogle Scholar
  38. Pimentel D, Lach L, Zuñiga R, Morrison D (2000) Environmental and economic costs associated to non-indigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  39. Pronzato R (1999) Sponge-fishing, disease and farming in the Mediterranean Sea. Aquat Conserv 9:485–493CrossRefGoogle Scholar
  40. Reiswig HM (1971) Particle feeding in natural populations of three marine demosponges. Biol Bull 141:568–591CrossRefGoogle Scholar
  41. Ribes M, Coma R, Atkinson MJ, Kinzie RA (2005) Sponges and ascidians control removal of particulate organic nitrogen from coral reef water. Limnol Oceanogr 50:1480–1489CrossRefGoogle Scholar
  42. 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 111–115Google Scholar
  43. Rützler K (1970) Spatial competition among Porifera: solution by epizoism. Oecologia 5:85–95CrossRefGoogle Scholar
  44. Schaffelke B, Hewitt CL (2007) Impacts of introduced seaweeds. Bot Mar 50:397–417Google Scholar
  45. 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 325:1–14CrossRefGoogle Scholar
  46. Simpson TL (1984) The cell biology of songes. Springer, New York, pp 517–523CrossRefGoogle Scholar
  47. Streftaris N, Zenetos A (2006) Alien Marine Species in the Mediterranean—the 100 ‘Worst Invasives’ and their Impact. Med Mar Sci 7:87–118Google Scholar
  48. 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 PubMedCrossRefGoogle Scholar
  49. Thomsen MS, Wernberg T, Tuya F, Silliman B (2009) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Phycol 45:812–819CrossRefGoogle Scholar
  50. 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 113:101–117CrossRefGoogle Scholar
  51. 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 124:159–170CrossRefGoogle Scholar
  52. Uriz MJ, Becerro MA, Tur JM, Turon X (1996) Location of toxicity within the Mediterranean sponge Crambe crambe (Demospongiae: Poecilosclerida). Mar Biol 124:583–590CrossRefGoogle Scholar
  53. 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 167:137–148CrossRefGoogle Scholar
  54. 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 259–270Google Scholar
  55. 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 516–524Google Scholar
  56. Verlaque M (1994) Inventaire des plantes introduites en Méditerranée: origines et répercussions sur l’environnement et les activités humaines. Oceanol Acta 17:1–23Google Scholar
  57. Whalan S, Battershill C, de Nys R (2007) Variability in reproductive output across a water quality gradient for a tropical marine sponge. Mar Biol 153:163–169CrossRefGoogle Scholar
  58. Wulff J (2006) Rapid diversity and abundance decline in a Caribbean coral reef sponge community. Biol Conserv 127:167–176CrossRefGoogle Scholar
  59. 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 13:2303–2308CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Centre d’Estudis Avançats de Blanes-CSICBlanes, GironaSpain
  2. 2.Departament de Ciències Ambientals, Facultat de CiènciesUniversitat de GironaGironaSpain

Personalised recommendations