Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Predator diversity and density affect levels of predation upon strongly interactive species in temperate rocky reefs

  • 256 Accesses

  • 27 Citations


Indirect effects of predators in the classic trophic cascade theory involve the effects of basal species (e.g. primary producers) mediated by predation upon strongly interactive consumers (e.g. grazers). The diversity and density of predators, and the way in which they interact, determine whether and how the effects of different predators on prey combine. Intraguild predation, for instance, was observed to dampen the effects of predators on prey in many ecosystems. In marine systems, species at high trophic levels are particularly susceptible to extinction (at least functionally). The loss of such species, which is mainly attributed to human activities (mostly fishing), is presently decreasing the diversity of marine predators in many areas of the world. Experimental studies that manipulate predator diversity and investigate the effects of this on strongly interactive consumers (i.e. those potentially capable of causing community-wide effects) in marine systems are scant, especially in the rocky sublittoral. I established an experiment that utilised cage enclosures to test whether the diversity and density of fish predators (two sea breams and two wrasses) would affect predation upon juvenile and adult sea urchins, the most important grazers in Mediterranean sublittoral rocky reefs. Changes in species identity (with sea breams producing major effects) and density of predators affected predation upon sea urchins more than changes in species richness per se. Predation upon adult sea urchins decreased in the presence of multiple predators, probably due to interference competition between sea breams and wrasses. This study suggests that factors that influence both fish predator diversity and density in Mediterranean rocky reefs (e.g. fishing and climate change) may have the potential to affect the predators’ ability to control sea urchin population density, with possible repercussions for the whole benthic community structure.

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

Fig. 1
Fig. 2a–b
Fig. 3a–b
Fig. 4


  1. Benedetti-Cecchi L (2004) Increasing accuracy of causal inference in experimental analyses of biodiversity. Funct Ecol 18:761–768

  2. Bulleri F, Benedetti-Cecchi L, Cinelli F (1999) Grazing by the sea urchin Arbacia lixula L. and Paracentrotus lividus Lmk in the Northwest Mediterranean. J Exp Mar Biol Ecol 241:81–95

  3. Bulleri F, Bertocci I, Micheli F (2002) Interplay of encrusting coralline algae and sea urchins in maintaining alternative habitats. Mar Ecol Progr Ser 243:101–109

  4. Cardinale BJ, Palmer MA, Collins SJ (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415:426–429

  5. Chapin FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Diaz S (2000) Consequences of changing biodiversity. Nature 405:234–242

  6. Dayton PK, Thrush SF, Agardy MT, Hofman RJ (1995) Ecosystem effects of marine fishing. Aquat Conserv: Mar Freshw Ecosys 5:205–232

  7. Downing AL, Leibold ME (2002) Ecosystem consequences of species richness and composition in pond food webs. Nature 416:837–841

  8. Duffy JE, Richardson JP, France KE (2005) Ecosystem consequences of diversity depend on chain length in estuarine vegetation. Ecol Lett 8:301–309

  9. Estes JA, Duggins DO (1995) Sea otters and kelp forests in Alaska: generality and variation in a community ecological paradigm. Ecol Monogr 65:75–100

  10. Fairwheather PG, Underwood AJ (1991) Experimental removals of a rocky intertidal predator: variations within two habitats in the effects on prey. J Exp Mar Biol Ecol 154:29–75

  11. Finke DL, Denno RF (2004) Predator diversity dampens trophic cascades. Nature 429:407–410

  12. Fowler-Walker MJ, Connell SD (2002) Opposing states of subtidal habitat across temperate Australia: consistency and predictability in kelp canopy-benthic associations. Mar Ecol Prog Ser 240:49–56

  13. Francour P, Boudouresque CF, Harmelin JG, Harmelin-Vivien ML, Quignard JP (1994) Are the Mediterranean waters becoming warmer? Information from biological indicators. Mar Poll Bull 28:523–536

  14. Froese R, Pauly D (2006) Fish Base. http://www.fishbase.org. Cited 20 August 2007

  15. Griffen BD (2006) Detecting emergent effects of multiple predator species. Oecologia 148:702–709

  16. Griffen BD, Byers JE (2006) Intraguild predation reduces redundancy of predator species in multiple predator assemblage. J Anim Ecol 75:959–966

  17. 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

  18. Guidetti P, Terlizzi A, Boero F (2004) Effects of the edible sea urchin, Paracentrotus lividus, fishery along the Apulian rocky coasts (SE Italy, Mediterranean Sea). Fish Res 66:287–297

  19. Guidetti P, Mori M (2005) Morpho-functional defences of Mediterranean sea urchins, Paracentrotus lividus and Arbacia lixula, against fish predators. Mar Biol 147:797–802

  20. Guidetti P (2006) Marine reserves re-establish lost predatory interactions and cause wide-community changes in rocky reefs. Ecol Appl 16:963–976

  21. Guidetti P, Dulcic J (2007) Relationships among predatory fish, sea urchins and barrens in Mediterranean rocky reefs across a latitudinal gradient. Mar Environ Res 63:168–184

  22. Guidetti P, Sala E (2007) Community-wide effects of marine reserves in the Mediterranean Sea. Mar Ecol Prog Ser 335:43–56

  23. Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinction? Trends Ecol Evol 19:470–474

  24. Halpern BS, Borer ET, Seabloom EW, Shurin JB (2005) Predator effects on herbivore and plant stability. Ecol Lett 8:189–194

  25. Harmelin JG, Bachet F, Garcia F (1995) Mediterranean marine reserves: fish indices as tests of protection efficiency. Mar Ecol 16:233–250

  26. Hereu B, Zabala M, Linares C, Sala E (2004) Temporal and spatial variability in settlement of the sea urchin Paracentrotus lividus in the NW Mediterranean. Mar Biol 144:1011–1018

  27. Hereu B, Zabala M, Linares C, Sala E (2005) The effects of predator abundance and habitat structural complexity on survival of juvenile sea urchins. Mar Biol 146:293–299

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

  29. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

  30. Hughes JB, Petchey OL (2001) Merging perspectives on biodiversity and ecosystem functioning. Trends Ecol Evol 16:222–223

  31. Ives AR, Cardinale BJ (2004) Food-web interactions govern the resistance of communities after non-random extinctions. Nature 429:174–177

  32. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes T, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

  33. Joliffe PA (2000) The replacement series. J Ecol 88:371–385

  34. Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808

  35. Micheli F, Benedetti-Cecchi L, Gambaccini S, Bertocci I, Borsini C, Osio GC, Romano F (2005) Alternate states, marine protected areas, and the structure of Mediterranean rocky-reef assemblages. Ecol Monogr 75:81–102

  36. Milazzo M, Anastasi I, Willis TJ (2006) Recreational fish feeding affects coastal fish behaviour and increases frequency of predation on damselfish Chromis chromis nests. Mar Ecol Prog Ser 310:165–172

  37. Montoya JM, Rodriguez MA, Hawkins BA (2003) Food web complexity and higher-level ecosystem services. Ecol Lett 6:587–593

  38. Naeem S, Thompson LJ, Lawler SP, Lawton JH, Woodfin RM (1994) Declining biodiversity can alter the performance of ecosystems. Nature 368:734–737

  39. O’Connor NE, Crowe TT (2005) Biodiversity loss and ecosystem functioning: distinguishing between number and identity of species. Ecology 86:1783–1796

  40. Pauly D, Christensen V, Dalsgaard J, Froese R, Torres FJ (1998) Fishing down marine food webs. Science 279:860–863

  41. Pinnegar JK, Polunin NVC, Francour P, Badalamenti F, Chemello R, Harmelin-Vivien ML, Hereu B, Milazzo M, Zabala M, D’Anna G, Pipitone C (2000) Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environ Conserv 27:179–200

  42. Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Ann Rev Ecol Syst 20:297–330

  43. 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

  44. 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

  45. Schmitz OJ (2003) Top-predator control of plant biodiversity and productivity in an old-field ecosystem. Ecol Lett 6:156–163

  46. Shears NT, Babcock RC (2002) Marine reserves demonstrate top-down control of community structure on temperate reefs. Oecologia 132:131–142

  47. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791

  48. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355

  49. Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579

  50. 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

  51. Tegner MJ, Dayton PK (2000) Ecosystem effects of fishing in kelp forest communities. ICES J Mar Sci 57:579–589

  52. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, Ferreira de Siquera M, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Townsend A, Peterson A, Phillips O, Williams SE (2004) Extinction risk from climate change. Nature 427:145–148

  53. Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720

  54. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845

  55. Underwood AJ (1993) Exploitation of species on the rocky coast of New South Wales (Australia) and options for its management. Ocean Coast Manag 20:41–62

  56. Underwood AJ (1997) Experiments in ecology: their logic design and interpretation using analysis of variance. Cambridge University Press, Cambridge

  57. Vance-Chalcraft HD, Soluk DA, Ozburn N (2004) Is prey predation risk influenced more by increasing predator density or predator species richness in steam enclosures? Oecologia 139:117–122

  58. Wilby A, Thomas MB (2002) Natural enemy diversity and pest control: patterns of pest emergence with agricultural intensification. Ecol Lett 5:353–360

  59. Witman JD, Dayton PK (2001) Rocky subtidal communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, MA, pp 339–366

  60. Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JB, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790

Download references


This paper represents a contribution towards the aims of MARBEF, an EU Network of Excellence on “Marine Biodiversity and Ecosystem Functioning” under EU-Framework Programme 6. The author benefited from a CNR (Italian National Centre for Research) fellowship in the framework of the “NATO-CNR senior fellowship programme 2002”. Many thanks are due to D.L. Finke, J. Stachowicz, E. Sala, L. Benedetti-Cecchi and F. Bulleri for their invaluable comments and suggestions on the manuscript. This paper is dedicated to little Elena, my baby, who recently come into the world.

Author information

Correspondence to Paolo Guidetti.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Guidetti, P. Predator diversity and density affect levels of predation upon strongly interactive species in temperate rocky reefs. Oecologia 154, 513–520 (2007). https://doi.org/10.1007/s00442-007-0845-5

Download citation


  • Multiple predator effects
  • Strongly interactive prey
  • Trophic cascades
  • Mediterranean rocky reefs
  • Manipulative experiments