Coral Reefs

, Volume 30, Issue 3, pp 827–837 | Cite as

Associational refuges among corals mediate impacts of a crown-of-thorns starfish Acanthaster planci outbreak

Indirect positive interactions in communities
  • Mohsen Kayal
  • Hunter S. Lenihan
  • Cédric Pau
  • Lucie Penin
  • Mehdi Adjeroud


Interactions among coral populations can moderate the impact of coral predator outbreaks, enhancing community resilience and recovery. This study used predator-exclusion cages and neighbour removals in a field experiment to test how indirect interactions between populations of three coral taxa, Acropora, Pocillopora, and Porites, influenced their survival during an outbreak of the crown-of-thorns starfish, Acanthaster planci, in Moorea, French Polynesia. High densities of corals enhanced survival by generating associational refuges: physical structures that impeded Acanthaster and protected corals, and by simple density-dependent prey dilution that reduced predation rates. Acanthaster showed feeding preferences, resulting in varying intensities of predation on corals, which (1) influenced the type and strength of the associational refuge among corals and (2) resulted in significant loss of the competitive dominants to the benefit of the competitive inferiors. The result was a set of indirect positive interactions (IPIs) that prevented Acanthaster from eradicating Acropora and may have enhanced Porites, a relatively weak competitor among corals. IPIs probably play a key role in many ecosystems, especially in coral reefs in which corals act as engineer species, to reduce impacts of perturbations and enhance community resilience. This study illustrates the importance of IPIs in community regulation with a new conceptual model.


Predation Mortality Habitat complexity Indirect positive interaction Community regulation Resilience 



The authors are grateful to Pauline Bosserelle, as well as to many volunteers from CRIOBE and Planète Urgence for assistance in the field, and to three anonymous reviewers for their critical comments on this manuscript. This study was supported by a grant from Société Polynésienne des Eaux et de l’Assainissement and Planète Urgence. H. Lenihan was supported by NSF (OCE0417412) and the Gordon and Betty Moore Foundation. This is another publication of the Moorea Coral Reef LTER.

Supplementary material

338_2011_763_MOESM1_ESM.pdf (10 kb)
ESM 1 Figure showing the density of Acanthaster planci on study site in Moorea, French Polynesia (PDF 11 kb)
338_2011_763_MOESM2_ESM.pdf (13 kb)
ESM 2 Protocol and results of the tests on the impact of caging treatments on light, mass water exchange, and sedimentation (PDF 13 kb)


  1. Adjeroud M, Pratchett MS, Kospartov MC, Lejeusne C, Penin L (2007) Small-scale variability in the size structure of scleractinian corals around Moorea, French Polynesia: patterns across depths and locations. Hydrobiologia 589:117–126CrossRefGoogle Scholar
  2. Adjeroud M, Chancerelle Y, Schrimm M, Perez T, Lecchini D, Galzin R, Salvat B (2005) Detecting the effects of natural disturbances on coral assemblages in French Polynesia: A decade survey at multiple scales. Aquat Living Resour 18:111–123CrossRefGoogle Scholar
  3. Adjeroud M, Michonneau F, Edmunds PJ, Chancerelle Y, Lison de Loma T, Penin L, Thibaut L, Vidal-Dupiol J, Salvat B, Galzin R (2009) Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a South Central Pacific reef. Coral Reefs 28:775–780CrossRefGoogle Scholar
  4. Altieri AH, Silliman BR, Bertness MD (2007) Hierarchical organization via a facilitation cascade in intertidal cordgrass bed communities. Am Nat 169:195–206CrossRefPubMedGoogle Scholar
  5. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193CrossRefPubMedGoogle Scholar
  6. Berumen ML, Pratchett MS (2006) Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea. Coral Reefs 25:647–653CrossRefGoogle Scholar
  7. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125CrossRefGoogle Scholar
  8. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965CrossRefGoogle Scholar
  9. Chesson P, Kuang JJ (2008) The interaction between predation and competition. Nature 456:235–238CrossRefPubMedGoogle Scholar
  10. Connell JH, Hughes TP, Walace CC, Tanner JE, Harms KE, Kerr AM (2004) A long-term study of competition and diversity of corals. Ecol Monogr 74:179–210CrossRefGoogle Scholar
  11. Cox EF (1986) The effects of a selective corallivore on growth rates and competition for space between two species of Hawaiian corals. J Exp Mar Biol Ecol 101:161–174CrossRefGoogle Scholar
  12. Crain CM, Bertness MD (2006) Ecosystem engineering across environmental gradients: implications for conservation and management. Bioscience 56:211–218CrossRefGoogle Scholar
  13. De’ath G, Moran PJ (1998) Factors affecting the behaviour of crown-of-thorns starfish (Acanthaster planci L.) on the Great Barrier Reef: 2: Feeding preferences. J Exp Mar Biol Ecol 220:107–126CrossRefGoogle Scholar
  14. Faure G (1989) Degradation of coral reefs at Moorea Island (French Polynesia) by Acanthaster planci. J Coast Res 5:295–305Google Scholar
  15. Grabowski JH, Hughes AR, Kimbro DL (2008) Habitat complexity influences cascading effects of multiple predators. Ecology 89:3413–3422CrossRefPubMedGoogle Scholar
  16. Gurevitch J, Morrison JA, Hedges LV (2000) The interaction between competition and predation: a meta-analysis of field experiments. Am Nat 155:435–453PubMedGoogle Scholar
  17. Hacker SD, Gaines SD (1997) Some implications of direct positive interactions for community species diversity. Ecology 78:1990–2003CrossRefGoogle Scholar
  18. Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77:950–963CrossRefGoogle Scholar
  19. Harriott VJ (1999) Coral growth in subtropical eastern Australia. Coral Reefs 18:281–291CrossRefGoogle Scholar
  20. Hughes TP, Connell JH (1987) Population dynamics based on size or age? A reef-coral analysis. Am Nat 129:818–829CrossRefGoogle Scholar
  21. Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957CrossRefGoogle Scholar
  22. Keesing JK, Lucas JS (1992) Field measurement of feeding and movement rates of the crown-of-thorns starfish Acanthaster planci (L.). J Exp Mar Biol Ecol 156:89–104CrossRefGoogle Scholar
  23. Kvitek RG, Oliver JS, DeGange AR, Anderson BS (1992) Changes in Alaskan soft-bottom prey communities along a gradient in sea otter predation. Ecology 73:413–428CrossRefGoogle Scholar
  24. Lenihan HS, Adjeroud M, Kotchen M, Hench J, Nakamura T (2008) Reef structure regulates small-scale spatial variation in coral bleaching. Mar Ecol Prog Ser 370:127–141CrossRefGoogle Scholar
  25. Levenbach S (2008) Community-wide ramifications of an associational refuge on shallow rocky reefs. Ecology 89:2819–2828CrossRefPubMedGoogle Scholar
  26. Levenbach S (2009) Grazing intensity influences the strength of an associational refuge on temperate reefs. Oecologia 159:181–190CrossRefPubMedGoogle Scholar
  27. Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition and predation in relation to environmental stress and recruitment. Am Nat 130:730–757CrossRefGoogle Scholar
  28. Michalet R, Brooker RW, Cavieres LA, Kikvidze Z, Lortie CJ, Pugnaire FI, Valiente-Banuet A, Callaway RM (2006) Do biotic interactions shape both sides of the humped-back model of species richness in plant communities? Ecol Lett 9:767–773CrossRefPubMedGoogle Scholar
  29. Milchunas DG, Noy-Meir I (2002) Grazing refuges, external avoidance of herbivory and plant diversity. Oikos 99:113–130CrossRefGoogle Scholar
  30. Paine RT (1974) Intertidal community structure. Experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia 15:93–120CrossRefPubMedGoogle Scholar
  31. Penin L, Adjeroud M, Pratchett MS, Hughes TP (2007) Spatial distribution of juvenile and adult corals around Moorea (French Polynesia): implications for population regulation. Bull Mar Sci 80:379–389Google Scholar
  32. Penin L, Michonneau F, Baird AH, Connolly SR, Pratchett MS, Kayal M, Adjeroud M (2010) Early post-settlement mortality and the structure of coral assemblages. Mar Ecol Prog Ser 408:55–64CrossRefGoogle Scholar
  33. Pratchett MS (2007) Feeding preferences of Acanthaster planci (Echinodermata: Asteroidea) under controlled conditions of food availability. Pac Sci 61:113–120CrossRefGoogle Scholar
  34. Pratchett MS, Schenk TJ, Baine M, Syms C, Baird AH (2009) Selective coral mortality associated with outbreaks of Acanthaster planci L. in Bootless Bay, Papua New Guinea. Mar Environ Res 67:230–236CrossRefPubMedGoogle Scholar
  35. Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Brashares JS (2009) The rise of the mesopredator. Bioscience 59:779–791CrossRefGoogle Scholar
  36. Rotjan RD, Lewis SM (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91CrossRefGoogle Scholar
  37. Sandin SA, Pacala SW (2005) Fish aggregation results in inversely density-dependent predation on continuous coral reefs. Ecology 86:1520–1530CrossRefGoogle Scholar
  38. Schmitt RJ, Holbrook SJ, Brooks AJ, Lape JCP (2009) Intraguild predation in a structured habitat: distinguishing multiple-predator effects from competitor effects. Ecology 90:2434–2443CrossRefPubMedGoogle Scholar
  39. Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Mohsen Kayal
    • 1
    • 2
  • Hunter S. Lenihan
    • 3
  • Cédric Pau
    • 1
    • 2
  • Lucie Penin
    • 2
    • 1
    • 4
  • Mehdi Adjeroud
    • 2
    • 5
  1. 1.USR 3278 CNRS-EPHE, Centre de Recherches Insulaires et Observatoire de l’EnvironnementPapetoai, MooreaFrench Polynesia
  2. 2.UMR 5244 CNRS-EPHE-UPVD, Biologie et Ecologie Tropicale et MéditerranéenneUniversité de Perpignan Via DomitiaPerpignan CedexFrance
  3. 3.Bren School of Environmental Science and ManagementUniversity of CaliforniaSanta BarbaraUSA
  4. 4.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  5. 5.Institut de Recherche pour le DéveloppementUnité 227 CoRéUs2 “Biocomplexité des écosystèmes coralliens de l’Indo-Pacifique”Nouméa CedexNew Caledonia

Personalised recommendations