Marine Biology

, Volume 158, Issue 10, pp 2267–2277 | Cite as

Mutualist-induced morphological changes enhance growth and survival of corals

  • Gerick S. BergsmaEmail author
  • Christopher M. Martinez
Original Paper


Species interactions can induce morphological changes in organisms that affect their subsequent growth and survival. In Moorea, French Polynesia, epibiotic gammaridean amphipods induce the formation of long, branch-like coral “fingers” on otherwise flat, encrusting, or plating Montipora coral colonies. The fingers form as corals encrust tubes built by the amphipods and lead to significant changes in colony morphology. This study examines the costs and benefits of this association to the amphipods and corals and demonstrates that the interaction is a mutualism. Amphipods gain protection from predators by living within corals, and corals benefit by enhanced growth and survival. Benefits to the coral arise through direct effects due to the amphipods’ presence as well as through benefits derived from the altered colony morphology. This study demonstrates that induced morphological plasticity can be a mechanism for facilitation, adding to our knowledge of the roles mutualism, and phenotypic plasticity play in ecology.


Coral Growth Reef Crest Finger Length Lateral Growth Rate Sand Patch 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Tom Adam, Nichole Price, Keith Seydel, and Jennifer Gowan for assistance in the field, William Rice for advice on the statistical analysis, and Sally Holbrook, Russell Schmitt, Gretchen Hofmann, Robin Pelc, Tamar Goulet, and two anonymous reviewers for helpful discussions and comments on the manuscript. This research was supported by a U.S. National Science Foundation grant (OCE 04-17412) and gifts from the Worster family and the Gordon and Betty Moore Foundation. This work is a contribution of the Moorea Coral Reef Long Term Ecological Research site, a component of the National Science Foundation’s Long Term Ecological Research Program and was conducted at the UC Berkeley Richard B. Gump South Pacific Research Station.


  1. Abelson A, Galil BS, Loya Y (1991) Skeletal modifications in stony corals caused by indwelling crabs: hydrodynamical advantages for crab feeding. Symbiosis 10:233–248Google Scholar
  2. Bergsma GS (2009) Tube-dwelling coral symbionts induce significant morphological change in Montipora. Symbiosis 49:143–150CrossRefGoogle Scholar
  3. Bertness MD, Leonard GH (1997) The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78:1976–1989CrossRefGoogle Scholar
  4. Bohannan BJM, Lenski RE (2000) The relative importance of competition and predation varies with productivity in a model community. Am Nat 156:329–340CrossRefGoogle Scholar
  5. Bradshaw AD, Caspari EW, Thoday JM (1965) Evolutionary significance of phenotypic plasticity in plants. In: Advances in genetics, vol 13. Academic Press, pp 115–155Google Scholar
  6. Carballo JL, Avila E, Enriquez S, Camacho L (2006) Phenotypic plasticity in a mutualistic association between the sponge Haliclona caerulea and the calcareous macroalga Jania adherens induced by transplanting experiments. I: Morphological responses of the sponge. Mar Biol 148:467–478CrossRefGoogle Scholar
  7. Chesson P, Huntley N (1997) The roles of harsh and fluctuating conditions in the dynamics of ecological communities. Am Nat 150:519–553CrossRefGoogle Scholar
  8. Dawkins R (1982) The extended phenotype: the gene as a unit of selection. Oxford University Press, New YorkGoogle Scholar
  9. DeWitt T, Scheiner S (eds) (2004) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, OxfordGoogle Scholar
  10. Dingemanse NJ, Oosterhof C, Van Der Plas F, Barber I (2009) Variation in stickleback head morphology associated with parasite infection. Biol J Linn Soc 96:759–768CrossRefGoogle Scholar
  11. Eldredge L, Kropp R (1982) Decapod crustacean-induced skeletal modification in Acropora. In: Gomez E, Birkeland C, Buddemeier R, Johannes R, Marsh J, Tsuda R (eds) Proceeding of the 4th International Coral Reef Symp, vol 2. Marine Science Center, University of the Philippines, Manila, pp 115–119Google Scholar
  12. Fernandez C, Boudouresque CF (1997) Phenotypic plasticity of Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Mar Ecol Prog Ser 152:145–154CrossRefGoogle Scholar
  13. Glynn PW (1976) Some physical and biological determinants of coral community structure in the Eastern Pacific. Ecol Monogr 46:431–456CrossRefGoogle Scholar
  14. Hetrick BAD (1991) Mycorrhizas and root architecture. Experientia 47:355–362CrossRefGoogle Scholar
  15. Hoeksema JD, Bruna EM (2000) Pursuing the big questions about interspecific mutualism: a review of theoretical approaches. Oecologia 125:321–330CrossRefGoogle Scholar
  16. Holbrook SJ, Brooks AJ, Schmitt RJ (2002) Variation in structural attributes of patch-forming corals and in patterns of abundance of associated fishes. Mar Freshwater Res 53:1045–1053CrossRefGoogle Scholar
  17. Kaniewska P, Anthony KRN, Hoegh-Guldberg O (2008) Variation in colony geometry modulates internal light levels in branching corals, Acropora humilis and Stylophora pistillata. Mar Biol 155:649–660CrossRefGoogle Scholar
  18. Krist AC (2000) Effect of the digenean parasite Proterometra macrostoma on host morphology in the freshwater snail Elimia livescens. J Parasitol 86:262–267CrossRefGoogle Scholar
  19. Lagrue C, McEwan J, Poulin R, Keeney DB (2007) Co-occurrences of parasite clones and altered host phenotype in a snail-trematode system. Int J Parasitol 37:1459–1467CrossRefGoogle Scholar
  20. Lamberts A (1978) Coral growth: alizarin method. In: Stoddart D, Johannes R (eds) Coral reefs: research methods. UNESCO, Paris, pp 523–527Google Scholar
  21. Liu PJ, Hsieh HL (2000) Burrow architecture of the spionid polychaete Polydora villosa in the corals Montipora and Porites. Zool Stud 39:47–54Google Scholar
  22. McCoy MW (2007) Conspecific density determines the magnitude and character of predator-induced phenotype. Oecologia 153:871–878CrossRefGoogle Scholar
  23. Menge BA, Sutherland JP (1976) Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. Am Nat 110:351–369CrossRefGoogle Scholar
  24. Meroz-Fine E, Shefer S, Ilan M (2005) Changes in morphology and physiology of an East Mediterranean sponge in different habitats. Mar Biol 147:243–250CrossRefGoogle Scholar
  25. Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692CrossRefGoogle Scholar
  26. Mokady O, Loya Y, Lazar B (1998) Ammonium contribution from boring bivalves to their coral host—a mutualistic symbiosis? Mar Ecol Prog Ser 169:295–301CrossRefGoogle Scholar
  27. Pellmyr O (1989) The cost of mutualism: interactions between Trollius europaeus and its pollinating parasites. Oecologia 78:53–59CrossRefGoogle Scholar
  28. Sandland GJ, Goater CP (2001) Parasite-induced variation in host morphology: brain-encysting trematodes in fathead minnows. J Parasitol 87:267–272CrossRefGoogle Scholar
  29. Sanford E, Roth MS, Johns GC, Wares JP, Somero GN (2003) Local selection and latitudinal variation in marine predator-prey interaction. Science 300:1135–1137CrossRefGoogle Scholar
  30. Shima JS, Osenberg CW, Stier AC (2010) The vermetid gastropod Dendropoma maximum reduces coral growth and survival. Biol Lett 6:815–818CrossRefGoogle Scholar
  31. Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246CrossRefGoogle Scholar
  32. Stachowicz JJ, Hay ME (1999) Mutualism and coral persistence: the role of herbivore resistance to algal chemical defense. Ecology 80:2085–2101CrossRefGoogle Scholar
  33. Stewart HL (2006) Morphological variation and phenotypic plasticity of buoyancy in the macroalga Turbinaria ornata across a barrier reef. Mar Biol 149:721–730CrossRefGoogle Scholar
  34. Stewart HL, Holbrook SJ, Schmitt RJ, Brooks AJ (2006) Symbiotic crabs maintain coral health by clearing sediments. Coral Reefs 25:609–615CrossRefGoogle Scholar
  35. Stone GN, Schonrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522CrossRefGoogle Scholar
  36. Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337CrossRefGoogle Scholar
  37. Trussell GC (1996) Phenotypic plasticity in an intertidal snail: the role of a common crab predator. Evolution 50:448–454CrossRefGoogle Scholar
  38. van Ommeren RJ, Whitham TG (2002) Changes in interactions between juniper and mistletoe mediated by shared avian frugivores: parasitism to potential mutualism. Oecologia 130:281–288CrossRefGoogle Scholar
  39. Via S (1993) Adaptive phenotypic plasticity: target or by-product of selection in a variable environment? Am Nat 142:352–365CrossRefGoogle Scholar
  40. Vytopil E, Willis BL (2001) Epifaunal community structure in Acropora spp. (Scleractinia) on the Great Barrier Reef: implications of coral morphology and habitat complexity. Coral Reefs 20:281–288CrossRefGoogle Scholar
  41. Zvuloni A, Armoza-Zvuloni R, Loya Y (2008) Structural deformation of branching corals associated with the vermetid gastropod Dendropoma maxima. Mar Ecol Prog Ser 363:103–108CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Ecology, Evolution and Marine BiologyUniversity of CaliforniaSanta BarbaraUSA
  2. 2.School of Marine and Atmospheric SciencesStony Brook UniversityStony BrookUSA
  3. 3.Division of Science and Environmental PolicyCalifornia State University Monterey BaySeasideUSA

Personalised recommendations