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Leading role of the sea urchin Arbacia lixula in maintaining the barren state in southwestern Mediterranean

Marine Biology volume 158, pages 2505–2513 (2011)Cite this article

Abstract

Sympatric sea urchin species are usually considered to belong to the same grazer guild. Nevertheless, their role in community dynamics may vary due to species-specific morphological traits, feeding preferences and foraging behavior. In the Mediterranean Sea, the two species Paracentrotus lividus and Arbacia lixula co-occur in barren areas. Whereas P. lividus is usually considered responsible for creating a barren ground, the roles of the two sea urchin species in its maintenance are currently unclear. The relative and combined effects of P. lividus and A. lixula on maintaining the benthic community in the barren state were tested experimentally, using orthogonal exclusion of the two species. Results show that exclusion of A. lixula, regardless of the presence of P. lividus, led to a significant decrease in the surface of bare rock and a significant change of the algal assemblages, thus demonstrating the major role of this species in maintaining the barren state.

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References

  • Airoldi L (2000) Responses of algae with different life histories to temporal and spatial variability of disturbance in subtidal reefs. Mar Ecol Prog Ser 195:81–92. doi:10.3354/meps195081

    Article  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. doi:10.1111/j.1442-9993.2001.01070.pp.x

    Google Scholar 

  • Anderson MJ, Robinson J (2003) Generalized discriminant analysis based on distances. Aust NZ J Stat 45:301–318

    Article  Google Scholar 

  • Andrew NL, Underwood AJ (1993) Density-dependent foraging in the sea urchin Centrostephanus rodgersii on shallow subtidal refs in New South Wales, Australia. Mar Ecol Prog Ser 99:89–98

    Article  Google Scholar 

  • Benedetti-Cecchi L, Cinelli F (1995) Habitat heterogeneity, sea urchin grazing and the distribution of algae in littoral rock pools on the west coast of Italy (western Mediterranean). Mar Ecol Prog Ser 126:203–212. doi:10.3354/meps126203

    Article  Google Scholar 

  • Benedetti-Cecchi L, Bulleri F, Cinelli F (1998) Density dependent foraging of sea urchins in shallow subtidal reefs on the west coast of Italy (western Mediterranean). Mar Ecol Prog Ser 163:203–211. doi:10.3354/meps163203

    Article  Google Scholar 

  • Blackstone NW (1998) Morphological, physiological and metabolic comparisons between runner-like and sheet-like inbred lines of a colonial hydroid. J Exp Biol 201:2821–2831

    CAS  PubMed  Google Scholar 

  • Bonaviri C, Vega Fernández T, Badalamenti F, Gianguzza P, Di Lorenzo M, Riggio S (2009) Relative role of fish vs. starfish predation in controlling sea urchin populations in Mediterranean rocky shores. Mar Ecol Prog Ser 382:129–138

    Article  Google Scholar 

  • Breitburg DL (1984) Residual effects of grazing: inhibition of competitor recruitment by encrusting coralline algae. Ecology 65:1136–1143

    Article  Google Scholar 

  • Breitburg DL (1985) Development of a subtidal epibenthic community: factors affecting species composition and the mechanisms of succession. Oecologia 65:173–184. doi:10.1007/BF00379215

    Article  Google Scholar 

  • Bulleri F, Benedetti-Cecchi L, Cinelli F (1999) Grazing by the sea urchins Arbacia lixula L. and Paracentrotus lividus Lam. in the Northwest Mediterranean. J Exp Mar Biol Ecol 24:81–95. doi:10.1016/S0022-0981(99)00073-8

    Article  Google Scholar 

  • Bulleri F, Bertocci I, Micheli F (2002) Interplay of encrusting coralline algae and sea urchins in maintaining alternative habitats. Mar Ecol Prog Ser 243:101–109. doi:10.3354/meps243101

    Article  Google Scholar 

  • Bulleri F, Tamburello L, Benedetti-Cecchi L (2009) Loss of consumers alters the effects of resident assemblages on the local spread of an introduced macroalga. Oikos 118:269–279. doi:10.1111/j.1600-0706.2008.16955.x

    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 Prog Ser 96:93–100

    Article  Google Scholar 

  • Dill LM, Heithaus MR, Walters CJ (2003) Behaviorally mediated indirect interactions in marine communities and their conservation implications. Ecology 84:1151–1157. doi:10.1890/0012-9658(2003)084[1151:BMIIIM]2.0.CO;2

    Article  Google Scholar 

  • Fanelli G, Piraino S, Belmonte G, Geraci S, Boero F (1994) Human predation along the Apulian rocky coast (SE Italy): desertification caused by Lithophaga lithophaga (Mollusca) fisheries. Mar Ecol Prog Ser 110:1–8

    Article  Google Scholar 

  • Fernández C, Boudouresque CF (1997) Phenotypic plasticity of Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Mar Ecol Prog Ser 152:145–154. doi:10.3354/meps152145

    Article  Google Scholar 

  • Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, Holling CS (2004) Regime shifts, resilience, and biodiversity in ecosystem management. Annu Rev Ecol Evol Syst 35:557–581. doi:10.1146/annurev.ecolsys.35.021103.105711

    Article  Google Scholar 

  • Frantzis A, Berthon JF, Maggiore F (1988) Relations trophique entre les oursin Arbacia lixula et Paracentrotus lividus (Echinoidea Regularia) et le phytobenthos infralittoral superficial dans la baie de Port-Cros (Var, rance). Sci Rep Port-Cros Nat Park Fr 14:81–140

    Google Scholar 

  • Freeman A (2006) Size-dependent trait-mediated indirect interactions among sea urchin herbivores. Behav Ecol 17:182–187. doi:10.1093/beheco/arj014

    Article  Google Scholar 

  • Gagnon P, Himmelman JH, Johnson LE (2004) Temporal variation in community interfaces: kelp-bed boundary dynamics adjacent to persistent urchin barrens. Mar Biol 144:1191–1203. doi:10.1007/s00227-003-1270-x

    Article  Google Scholar 

  • Gianguzza P, Chiantore M, Bonaviri C, Cattaneo-Vietti R, Vielmini I, Riggio S (2006) The effects of recreational Paracentrotus lividus fishing on distribution patterns of sea urchins at Ustica Island MPA (Western Mediterranean, Italy). Fish Res 81:37–44. doi:10.1016/j.fishres.2006.06.002

    Article  Google Scholar 

  • Gianguzza P, Bonaviri C, Milisenda G, Barcellona A, Agnetta D, Vega Fernández T, Badalamenti F (2010) Macroalgal assemblage type affects predation pressure on sea urchins by altering adhesion strength. Mar Environ Res 70:82–86. doi:10.1016/j.marenvres.2010.03.006

    Article  CAS  Google Scholar 

  • Guidetti P (2006) Marine reserves reestablish lost predatory interactions and cause community changes in rocky reefs. Ecol Appl 16:963–976. doi:10.1890/1051-0761(2006)016[0963:MRRLPI]2.0.CO;2

    Article  Google Scholar 

  • Guidetti P, Dulčić J (2007) Relationship among predatory fish, sea urchins and barrens in Mediterranean rocky reefs across a latitudinal gradient. Mar Environ Res 63:168–184. doi:10.1016/j.marenvres.2006.08.002

    Article  CAS  Google Scholar 

  • Guidetti P, Fraschetti S, Terlizzi A, Boero F (2003) Distribution patterns of sea urchins and barrens in shallow Mediterranean rocky reefs impacted by the illegal fishery of the rock-boring mollusc Lithophaga lithophaga. Mar Biol 143:1135–1142. doi:10.1007/s00227-003-1163-z

    Article  Google Scholar 

  • Hereu B (2006) Depletion of palatable algae by sea urchins and fishes in a Mediterranean subtidal community. Mar Ecol Prog Ser 313:95–103. doi:10.3354/meps313095

    Article  Google Scholar 

  • Hereu B, Zabala M, Sala E (2008) Multiple controls of community structure and dynamics in a sublittoral marine environment. Ecology 89:3423–3435. doi:10.1890/07-0613.1

    Article  Google Scholar 

  • Jackson JBC (1979) Morphological strategies of sessile animals. In: Larwood G, Rosen B (eds) Biology and systematics of colonial animals. Academic Press, London, pp 499–556

    Google Scholar 

  • Johnson CR, Mann KH (1986) The crustose coralline alga, Phymatolithon Foslie, inhibits the overgrowth of seaweeds without relying on herbivores. J Exp Mar Biol Ecol 96:127–146. doi:10.1016/0022-0981(86)90238-8

    Article  Google Scholar 

  • Johnson CR, Mann KH (1988) Diversity, patterns of adaptation, and stability of Nova Scotia kelp beds. Ecol Monogr 58:129–154

    Article  Google Scholar 

  • Kempf M (1962) Recherchs d’ècologie comparée sur Paracentrotus lividus (Lmk.) et Arbacia lixula (L.). Rec Trav Stn Mar Endoume Fac Sci Mars 25:47–116

    Google Scholar 

  • Knowlton N (2004) Multiple “stable” states and the conservation of marine ecosystems. Progr Oceanogr 60:387–396. doi:10.1016/j.pocean.2004.02.011

    Article  Google Scholar 

  • Lauzon-Guay J-S, Scheibling RE (2007) Behaviour of sea urchin (Strongylocentrotus droebachiensis) grazing fronts: food-mediated aggregation and density-dependent facilitation. Mar Ecol Prog Ser 329:191–204. doi:10.3354/meps329191

    Article  Google Scholar 

  • Levitan DR, Sewell MA, Chia FS (1992) How distribution and abundance influence fertilization success in the sea urchin Strongylocentotus franciscanus. Ecology 13:248–254

    Article  Google Scholar 

  • Ling SD, Johnson CR, Frusher S, Ridgwa K (2009) Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. PNAS 106:22341–22345. www.pnas.org/cgi/doi/10.1073/pnas.0907529106

    Article  CAS  Google Scholar 

  • Ling SD, Ibbott S, Sanderson JC (2010) Recovery of canopy-forming macroalgae following removal of the enigmatic grazing sea urchin Heliocidaris erythrogramma. J Exp Mar Biol Ecol 395:135–146. doi:10.1016/j.jembe.2010.08.027

    Article  Google Scholar 

  • Micheli F, Benedetti-Cecchi L, Gambaccini S, Bertocci I, Borsini C, Chato Osio G, Romano F (2005) Cascading human impacts, marine protected areas, and the structure of Mediterranean reef assemblages. Ecol Monogr 75:81–102. doi:10.1890/03-4058

    Article  Google Scholar 

  • Palacín C, Giribet G, Carner S, Dantart L, Turin X (1998) Low density of sea urchins influence the structure of algal assemblages in the western Mediterranean. J Sea Res 39:281–290

    Article  Google Scholar 

  • Petraitis PS, Dudgeon SR (2004) Detection of alternative stable states in marine communities. J Exp Mar Biol Ecol 300:343–371. doi:10.1016/j.jembe.2003.12.026

    Article  Google Scholar 

  • Privitera D, Chiantore M, Mangialajo L, Glavic N, Kozul W, Cattaneo-Vietti R (2008) Inter- and intra-specific competition between Paracentrotus lividus and Arbacia lixula in resource-limited barren areas. J Sea Res 60:184–192. doi:10.1016/j.seares.2008.07.001

    Article  Google Scholar 

  • Régis MB (1979) Particularités microstructurales du squelette de Paracentrotus lividus et Arbacia lixula: rapports avec l’écologie et l’éthologie de ces échinoïdes. Mar Biol 54:373–382

    Article  Google Scholar 

  • Sala E, Zabala M (1996) Fish predation and the structure of the sea urchin Paracentrotus lividus populations in the NW Mediterranean. Mar Ecol Prog Ser 140:71–81. doi:10.3354/meps140071

    Article  Google Scholar 

  • Sala E, Boudouresque CF, Harmelin-Vivien M (1998) Fishing, trophic cascades, and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 82:425–439

    Article  Google Scholar 

  • Shears NT, Babcock RC (2002) Marine reserves demonstrate top-down control of community structure on temperate reef. Oecologia 132:131–142. doi:10.1007/s00442-002-0920-x

    Article  Google Scholar 

  • Shears NT, Babcock RC, Salomon AK (2008) Context-dependent effects of fishing: variation in trophic cascades across environmental gradients. Ecol Appl 18:1860–1873

    Article  Google Scholar 

  • Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498

    Article  Google Scholar 

  • Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459. doi:10.1017/S0376892902000322

    Article  Google Scholar 

  • Suding KN, Gross KL, Houseman GR (2004) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:46–53. doi:10.1016/j.tree.2003.10.005

    Article  Google Scholar 

  • Verlaque M (1987) Relations entre Paracentrotus lividus (Lamarck) et le phytobenthos de Mediterranee occidentale. In: Boudoresque CF (ed) Colloque International sur Paracentrotus lividus et les oursins comestibles. GIS Posidonie Publication, Marseille, pp 5–36

    Google Scholar 

  • Verlaque M, Nedelec H (1983) Biologie de Paracentrotus lividus sur substrat rocheux en Corse (Mediterranee, France): alimentation des adultes. Vie Milieu 33:191–201

    Google Scholar 

  • Wright JT, Dworjanyn SA, Rogers CN, Steinberg PD, Williamson JE, Poore AGB (2005) Density-dependent sea urchin grazing: differential removal of species, changes in community composition and alternative community states. Mar Ecol Prog Ser 298:143–156. doi:10.3354/meps298143

    Article  Google Scholar 

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Acknowledgments

This work is dedicated to the late O. Daniela Saracino, whose kind and patient teaching was an essential legacy. The authors wish to thank Davide Agnetta, Andrea Barcellona, Manfredi Di Lorenzo, Francesco Di Trapani, Davide Perricone, Fernando Rubino and Clauda Scianna for their assistance in the field experiments and Giuseppe Portacci for his assistance in image analysis. The authors are indebted to Julie-Anne Buck for revising the English text. Three anonymous reviewers greatly improved the manuscript. This study was funded by the MPA “Isola di Ustica” and the Italian Ministry of the Environment and Protection of the Territory (MATT).

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Authors and Affiliations

  1. Dipartimento di Scienze della Terra e del Mare, Università di Palermo, Via Archirafi 18, 90123, Palermo, Italy

    C. Bonaviri & P. Gianguzza

  2. Laboratorio di Ecologia Marina, CNR—IAMC, Via G. da Verrazzano 17, 91014, Castellammare del Golfo, TP, Italy

    T. Vega Fernández & F. Badalamenti

  3. Talassografico “A. Cerruti”, CNR—IAMC, Via Roma 3, 74123, Taranto, Italy

    G. Fanelli

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  1. C. Bonaviri
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  2. T. Vega Fernández
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  3. G. Fanelli
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  4. F. Badalamenti
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  5. P. Gianguzza
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Correspondence to C. Bonaviri.

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Communicated by F. Bulleri.

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Bonaviri, C., Vega Fernández, T., Fanelli, G. et al. Leading role of the sea urchin Arbacia lixula in maintaining the barren state in southwestern Mediterranean. Mar Biol 158, 2505–2513 (2011). https://doi.org/10.1007/s00227-011-1751-2

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  • DOI: https://doi.org/10.1007/s00227-011-1751-2

Keywords

  • Benthic Community
  • Barren Area
  • Crustose Coralline Alga
  • Bare Rock
  • Benthic Assemblage