Abstract
Asteroids are largely recognized as important predators in all of the world’s oceans and for this reason, they play a crucial role in shaping the structure and functioning of benthic ecosystems. The spiny starfish Marthasterias glacialis is generally considered a voracious predator of molluscs, in particular bivalves. Using field observations and carbon (δ13C) and nitrogen (δ15N) stable isotopes, we explored possible changes in diet in relation to size of M. glacialis. Data were collected at Ustica Island (Southern Tyrrhenian Sea) from June 2008 to June 2010. M. glacialis showed a size shift in feeding preferences due to different use of food items: bivalves, Columbella rustica, Euthria cornea and Trochoidea were strongly selected by small starfish whereas the larger ones preferred Arbacia lixula and Paracentrotus lividus. The clear picture that emerged is that large M. glacialis is able to control sea urchin populations and indirectly Mediterranean rocky reef ecosystems.
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References
Abitia-Cardenas LA, Galvan-Magaña F, Gutierrez-Sanchez FJ, Rodriguez-Romero J, Aguilar-Palomino B, Moehl-Hitz A (1999) Diet of blue marlin Makaira mazara off the coast of Cabo San Lucas, Baja California Sur, Mexico. Fish Res 44(1):95–100
Agnetta D, Bonaviri C, Badalamenti F, Scianna C, Vizzini S, Gianguzza P (2013) Functional traits of two co-occurring sea urchins across a barren/forest patch system. J Sea Res 76:170–177
Agnetta D, Badalamenti F, Ceccherelli G, Di Trapani F, Bonaviri C, Gianguzza P (2015) Role of two co-occurring Mediterranean sea urchins in the formation of barren from Cystoseira canopy. Estuar Coast Mar Sci 152:73–77
Bacha M, Amara R (2012) Inter-cohort differences in growth, condition and feeding of juvenile anchovy (Engraulis encrasicolus) in the Gulf of Bejaia (Algerian coast, SW Mediterranean): implications for recruitment success. Fish Res 129:73–81
Berg J (1979) Discussion of methods of investigating the food of fishes, with reference to a preliminary study of the prey of Gobiusculus flavescens (Gobiidae). Mar Biol 50:263–273
Bonaviri C, Fernandez TV, Badalamenti F, Gianguzza P, Di Lorenzo M, Riggio S (2009) Fish versus starfish predation in controlling sea urchin populations in Mediterranean rocky shores. Mar Ecol Prog Ser 382:129–138
Bonaviri C, Fernandez TV, Fanelli G, Badalamenti F, Gianguzza P (2011) Leading role of the sea urchin Arbacia lixula in maintaining the barren state in southwestern Mediterranean. Mar Biol 158(11):2505–2513
Bonaviri C, Gianguzza P, Pipitone C, Hereu B (2012) Micropredation on sea urchins as a potential stabilizing process for rocky reefs. J Sea Res 73:18–23
Branch GM (1978) The responses of south african patellid limpets to invertebrate predators. Zool Afr 13(2):221–232
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 241(1):81–95
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
Chintiroglou C, Koukouras A (1991) Observations on the feedings habits of Calliactis parasitica (Couch, 1842), Anthozoa, Cnidaria. Oceanol Acta 14:389–396
Clarke KR, Gorley RN (2006) Primer v6: user manual/tutorial. Primer-E, Plymouth
Clarke KR, Somerfield PJ, Gorley RN (2008) Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Biol Ecol 366:56–69
Colombo F, Costa V, Dubois SF, Gianguzza P, Mazzola A, Vizzini S (2013) Trophic structure of vermetid reef community: high trophic diversity at small spatial scales. J Sea Res 77:93–99
Dance C, Savy S (1987) Predation on Paracentrotus lividus by Marthasterias glacialis: an in situ experiment at Port-Cros (France, Mediterranean). Posidonia Newsl 1(2):35–41
Di Trapani F, Aglieri G, Badalamenti F, Bonaviri C, Gianguzza P, Riggio S (2009) Distribution and diet of Marthasterias glacialis at Ustica Island MPA. Biol Mar Medit 16(1):262–263
Duggins DO (1983) Starfish predation and the creation of mosaic patterns in a kelp-dominated community. Ecology 64(6):1610–1619
Ebling FJ, Hawkins AD, Kitching FA, Muntz I, Pratt VM (1966) The ecology of Lough Hyne. XVI. Predation and diurnal migration in the Paracentrotus population. J Anim Ecol 35:559–566
Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC et al (2011) Trophic downgrading of planet earth. Science 333(6040):301–306
Fanelli G, Piraino S, Esposito L, Boero F (1999) Opposite roles of sea urchins and starfishes in marine benthic communities. In: Carnevali C, Bonasoro F (eds) Echinoderm research. Balkema, Rotterdam, pp 453–457
Forster GR (1962) Observations on the ormer population of Guernsey. Haliotis tuberculata (Gastropoda). J Mar Biol Assoc U K 42(3):493–498
Freeman A (2006) Size-dependent trait-mediated indirect interactions among sea urchin herbivores. Behav Ecol 17(2):182–187
Frid CLJ (1992) Foraging behavior of the spiny starfish Marthasterias glacialis in Lough Ine, Co Cork. Mar Behav Physiol 19(4):227–239
Galasso NM, Bonaviri C, Di Trapani F, Picciotto M, Gianguzza P, Agnetta D, Badalamenti F (2015) Fish-seastar facilitation leads to algal forest restoration on protected rocky reefs. Sci Rep 5:12409. doi:10.1038/srep12409
Gaymer CF, Himmelman JH (2008) A keystone predatory sea star in the intertidal zone is controlled by a higher-order predatory sea star in the subtidal zone. Mar Ecol Prog Ser 370:143–153
Gaymer CF, Dutil C, Himmelman JH (2004) Prey selection and predatory impact of four major sea stars on a soft bottom subtidal community. J Exp Mar Biol Ecol 313(2):353–374
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(1):37–44
Gianguzza P, Bonaviri C, Guidetti P (2009a) Crushing predation of the spiny star Marthasterias glacialis upon the sea urchin Paracentrotus lividus. Mar Biol 156(5):1083–1086
Gianguzza P, Badalamenti F, Gianguzza F, Bonaviri C, Riggio S (2009b) The operational sex ratio of the sea urchin Paracentrotus lividus populations: the case of the Mediterranean marine protected area of Ustica Island (Tyrrhenian Sea, Italy). Mar Ecol-Evol Persp 30(1):125–132
Gianguzza P, Bonaviri C, Milisenda G, Barcellona A, Agnetta D, Fernandez TV, Badalamenti F (2010) Macroalgal assemblage type affects predation pressure on sea urchins by altering adhesion strength. Mar Environ Res 70(1):82–86
Gianguzza P, Di Trapani F, Bonaviri C, Visconti G, Deidun A, Badalamenti F (2015) New body metrics to determine asteroid size and weight directly in the field. Thalassas 31(1):73–82
Griffiths RJ (1981) Predation on the bivalve Choromytilus meridionalis by the gastropod Natica tecta. J Molluscan Stud 47(1):112–120
Guidetti P (2004) Consumers of sea urchins, Paracentrotus lividus and Arbacia lixula, in shallow Mediterranean rocky reefs. Helgol Mar Res 58(2):110–116
Guidetti P (2006) Estimating body size of sea urchins, Paracentrotus lividus and Arbacia lixula, from stomach contents of Diplodus sargus, a Mediterranean predatory fish. J Appl Ichthyol 22(1):91–93
Guidetti P, Mori M (2005) Morpho-functional defences of Mediterranean sea urchins, Paracentrotus lividus and Arbacia lixula, against fish predators. Mar Biol 147(3):797–802
Guidetti P, Sala E (2007) Community-wide effects of marine reserves in the Mediterranean Sea. Mar Ecol Prog Ser 335:43–56
Guillou M (1996) Biotic and abiotic interactions controlling starfish outbreaks in the Bay of Douarnenez, Brittany, France. Oceanol Acta 19(3–4):415–420
Guler M, Lok A (2015) Foraging behaviors of sea stars, Marthasterias glacialis and Astropecten aranciacus (Asteroidea) and predator-prey interactions with warty venus clam, Venus verrucosa (Bivalvia). J Exp Mar Biol Ecol 465:99–106
Hyslop E (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17(4):19
Ivlev VS (1961) Experimental ecology of the feeding of fishes. Yale University Press, New Haven
Kempf M (1962) Recherches d’écologie compareé sur Paracentrotus lividus et Arbacia lixula. Rec Trav St Mar Endoume 25:47–116
Kitching JA, Thain VM (1983) The ecological impact of the sea urchin Paracentrotus lividus (Lamarck) in Lough Ine, Ireland. Philos Trans R Soc Lond 300(B):513–552
Krebs CJ (1989) Ecological methodology. Harper and Row, New York
La Mesa G, Vacchi M (1999) An analysis of the coastal fish assemblage of the Ustica Island marine reserve (Mediterranean Sea). Mar Ecol PSZNI 20(2):147–165
Labropoulou M, Eleftheriou A (1997) The foraging ecology of two pairs of congeneric demersal fish species: importance of morphological characteristics in prey selection. J Fish Biol 50(2):324–340
Lawrence JM (1992) Arm loss and regeneration in Asteroidea (Echinodermata). Echinoderm Res 1991:39–52
Lawrence JM, Larrain A (1994) The cost of arm autotomy in the starfish Stichaster striatus. Mar Ecol Prog Ser 109(2–3):311–313
Magennis B (1981) Feeding habits of Marthasterias glacialis (L). J Sherkin Isl 1(2):27–34
Magnesen T, Redmond KJ (2012) Potential predation rates by the sea stars Asterias rubens and Marthasterias glacialis, on juvenile scallops, Pecten maximus, ready for sea ranching. Aquac Int 20(1):189–199
McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102(2):378–390
Milazzo M, Chemello R, Badalamenti F, Riggio S (2000) Molluscan assemblages associated with photophilic algae in the Marine Reserve of Ustica Island (Lower Tyrrhenian Sea, Italy). Ital J Zool 67(3):287–295
O’Sullivan D, Emmerson M (2011) Marine reserve designation, trophic cascades and altered community dynamics. Mar Ecol Prog Ser 440:115–128
Paine RT (1974) Intertidal community structure. Oecologia 15:93–120
Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5(3):e9672. doi:10.1371/journal.pone.0009672
Penney AJ, Griffiths CL (1984) Prey selection and the impact of the starfish Marthasterias glacialis (L.) and other predators on the mussel Choromytilus meridionalis (Krauss). J Exp Mar Biol Ecol 75(1):19–36
Pérez-Portela R, Villamor A, Almada V (2010) Phylogeography of the sea star Marthasterias glacialis (Asteroidea, Echinodermata): deep genetic divergence between mitochondrial lineages in the north-western mediterranean. Mar Biol 157:2015–2028
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320
Pratchett MS (2005) Dynamics of an outbreak population of Acanthaster planci at Lizard Island, northern Great Barrier Reef (1995–1999). Coral Reefs 24(3):453–462
Pratchett MS (2007) Feeding preferences of Acanthaster planci (Echinodermata: Asteroidea) under controlled conditions of food availability. Pac Sci 61(1):113–120
Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Brashares JS (2009) The rise of the mesopredator. Bioscience 59(9):779–791
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Riggio S, Milazzo M (2004) Ricchezza specifica e biodiversità marina nell'isola di Ustica. Naturalista siciliano 28:559–586
Rodriguez RS, Ojeda FP (1998) Behavioral responses of the sea urchin Tetrapygus niger to predators and food. Mar Freshw Behav Physiol 31(1):21–37
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(1–3):71–81
Sarà G, Lo Martire M, Sanfilippo M, Pulicano G, Cortese G, Mazzola A, Manganaro A, Pusceddu A (2011) Impacts of marine aquaculture at large spatial scales: evidences from N and P catchment loading and phytoplankton biomass. Mar Environ Res 71(5):317–324
Savy S (1987) Activity pattern of the sea-star, Marthasterias glacialis, in Port-Cros Bay (France, mediterranean coast). Mar Ecol PSZNI 8(2):97–106
Schroeter SC, Dixon J, Kastendiek J (1983) Effects of the starfish Patiria miniata on the distribution of the sea urchin Lytechinus anamesus in a southern Californian kelp forest. Oecologia 2:141–147
Tomas F, Alvarez-Cascos D, Turon X, Romero J (2006) Differential element assimilation by sea urchins Paracentrotus lividus in seagrass beds: implications for trophic interactions. Mar Ecol Prog Ser 306:125–131
Tuya F, Duarte P (2012) Role of food availability in the bathymetric distribution of the starfish Marthasterias glacialis (Lamk.) on reefs of northern Portugal. Scientia Marina 76(1):9–15
Valinassab T, Jalali S, Hafezieh M, Zarshenas G (2011) Evaluation of some feeding indices of Pomadasys kaakan in the Northern Persian Gulf. Iran J Fish Sci 10(3):497–504
Verlaque MV (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, Marseille, pp 5–36
Verling E, Crook AC, Barnes DKA, Harrison SSC (2003) Structural dynamics of a sea-star (Marthasterias glacialis) population. J Mar Biol Assoc UK 83(3):583–592
Acknowledgments
N. Galasso and G. Aglieri significantly contributed to field sampling. Sample pre-treatment for stable isotope analysis was carried out by A. Mirasole and S. Noè, while isotopic analysis was performed by A. E. Aleo. Special thanks to Renato Chemello, Giovanni Fanelli and the anonymous reviewer for their constructive and challenging comments, which substantially improved this manuscript. Michelle Bowri revisited the English text. Chiara Bonaviri was supported by the Italian project FIRB (Contract No. RBFR12RXW). This study was funded by the research project “Monitoraggio delle popolazioni di Paracentrotus lividus e Arbacia lixula ai fini della tutela della diversità biologica dell’AMP Isola di Ustica”, under the Italian Ministry of the Environment (M.A.T.T.M - Ministero dell’Ambiente e della Tutela del Territorio e del Mare), University of Palermo (FFR 2012-13) and by the Flagship Project RITMARE – Italian Research for the Sea - funded by the Italian Ministry of Education, University and Research.
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Sampling was conducted under a research permit from MPA management body of the Ustica Island (Port Authority of Palermo). All authors approved the final version of the manuscript, and consent to submit has been received from all co-authors. The authors declare no competing financial interests or conflict of interest.
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Gianguzza, P., Di Trapani, F., Bonaviri, C. et al. Size-dependent predation of the mesopredator Marthasterias glacialis (L.) (Asteroidea). Mar Biol 163, 65 (2016). https://doi.org/10.1007/s00227-016-2835-9
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DOI: https://doi.org/10.1007/s00227-016-2835-9