Marine Biology

, Volume 162, Issue 8, pp 1523–1530 | Cite as

Vermetid gastropods mediate within-colony variation in coral growth to reduce rugosity

  • Jeffrey S. Shima
  • Daniel McNaughtan
  • Amanda T. Strong
Original Paper


Intraspecific variation in coral colony growth forms is common and often attributed to phenotypic plasticity. The ability of other organisms to induce variation in coral colony growth forms has received less attention, but has implications for both taxonomy and the fates of corals and associated species (e.g. fishes and invertebrates). Variation in growth forms and photochemical efficiency of massive Porites spp. in lagoons of Moorea, French Polynesia (17.48°S, 149.85°W), were quantified in 2012. The presence of a vermetid gastropod (Ceraesignum maximum) was correlated with (1) reduced rugosity of coral colonies and (2) reduced photochemical efficiency (Fv/Fm) on terminal “hummocks” (coral tissue in contact with vermetid mucus nets) relative to adjacent “interstitial” locations (tissue not in contact vermetid mucus nets). A manipulative field experiment confirmed that the relative growth rate of coral tissue was greater in interstices than hummocks when vermetids were present and similar (but with a trend for faster growth on hummocks) when vermetids were absent. Collectively, these results indicate that vermetid gastropods interact (presumably via their mucus nets) with coral colony architecture to impair photochemical efficiency, reduce growth rates of specific portions of a coral tissue, and induce a smoothed colony morphology. Given that structural complexity of coral colonies is an important determinant of “habitat quality” for many other species (fishes and invertebrates), these results suggest that the vermetid gastropod, C. maximum (with a widespread distribution and reported increases in density in some portions of its range), may have important indirect effects on many coral-associated organisms.


Coral Tissue Photochemical Efficiency Coral Coloni Coral Growth Coral Rubble 
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.



Funding was provided by grants from Victoria University of Wellington and NSF (OCE-1130359). We acknowledge UC Berkeley Gump Research Station for logistic support. This is Contribution Number 212 from UC Berkeley’s Richard B. Gump South Pacific Research Station, Moorea, French Polynesia.


  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. Aeby GS, Williams GJ, Franklin EC, Haapkyla J, Harvell CD, Neale S, Page CA, Raymundo L, Vargas-Angel B, Willis BL, Work TM, Davy SK (2011) Growth anomalies on the coral genera Acropora and Porites are strongly associated with host density and human population size across the Indo-Pacific. Plos One 6:e16887CrossRefGoogle Scholar
  3. Bergsma GS (2009) Tube-dwelling coral symbionts induce significant morphological change in Montipora. Symbiosis 49:143–150CrossRefGoogle Scholar
  4. Bergsma GS (2012) Coral mutualists enhance fish abundance and diversity through a morphology-mediated facilitation cascade. Mar Ecol Prog Ser 451:151–161CrossRefGoogle Scholar
  5. Bruno JF, Edmunds PJ (1997) Clonal variation for phenotypic plasticity in the coral Madracis mirabilis. Ecology 78:2177–2190CrossRefGoogle Scholar
  6. Chappell J (1980) Coral morphology, diversity and reef growth. Nature 286:249–252CrossRefGoogle Scholar
  7. Colgan MW (1985) Growth rate reduction and modification of a coral colony by a vermetid mollusc, Dendropoma maxima. Proceedings of the 5th international coral reef symposium 6:205–210Google Scholar
  8. Connell JH (1976) Competitive interactions and the species diversity of corals. In: Mackie GO (ed) Coelenterate ecology and behavior. Plenum Press, New York, pp 51–68CrossRefGoogle Scholar
  9. Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weight technique. Mar Biol 101:389–395CrossRefGoogle Scholar
  10. Dustan P (1975) Growth and form in the reef-building coral Montastrea annularis. Mar Biol 33:101–107CrossRefGoogle Scholar
  11. Edmunds PJ (2009) Effect of acclimatization to low temperature and reduced light on the response of reef corals to elevated temperature. Mar Biol 156:1797–1808CrossRefGoogle Scholar
  12. Forsman ZH, Barshis DJ, Hunger CL, Toonen RJ (2009) Shape-shifting corals: molecular markers show morphology is evolutionarily plastic in Porites. BMC Evol Biol 9:45CrossRefGoogle Scholar
  13. Fukami H, Budd AF, Paulay G, Sole-Cava A, Chen CA, Iwao K, Knowlton N (2004) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427:832–835CrossRefGoogle Scholar
  14. Geange SW, Stier AC (2009) Order of arrival affects competition in two reef fishes. Ecology 90:2868–2878CrossRefGoogle Scholar
  15. Gladfelter WB, Gladfelter EH (1978) Fish community structure as a function of habitat structure on West Indian patch reefs. Rev Biol Trop 26:65–84Google Scholar
  16. Golding RE, Bieler R, Rawlings TA, Collins TM (2014) Deconstructing Dendropoma: a systematic revision of a world-wide worm-snail roup, with descriptions of new genera (Caenogastropoda: Vermetidae). Malacologia 57:1–97CrossRefGoogle Scholar
  17. Graham NAJ, Wilson SK, Pratchett MS, Polunin NVC, Spalding MD (2009) Coral mortality versus structural collapse as drivers of corallivorous butterflyfish decline. Biodivers Conserv 18:3325–3336CrossRefGoogle Scholar
  18. Holbrook SJ, Schmitt RJ (2002) Competition for shelter space causes density-dependent predation mortality in damselfishes. Ecology 83:2855–2868CrossRefGoogle Scholar
  19. Kappner I, Al-Moghrabi SM, Richter C (2000) Mucus-net feeding by the vermetid gastropod Dendropoma maxima in coral reefs. Mar Ecol Prog Ser 204:309–313CrossRefGoogle Scholar
  20. Kayal M, Vercelloni J, Lison de Loma T, Bosserelle P, Chancerelle Y, Geoffroy S, Stievenart Céline, Michonneau F, Penin L, Planes S, Adjeroud M (2012) Predator Crown-of-Thorns starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities. PLoS ONE 7(10):e47363CrossRefGoogle Scholar
  21. Lang JC (1973) Interspecific aggression by scleractinian corals. II. Why the race is not always to the swift. Bull Mar Sci 23:260–279Google Scholar
  22. Lesser MP, Weis VM, Patterson MR, Jokiel PL (1994) Effects of morphology and water motion on carbon delivery and productivity in the reef coral, Pocillopora damicornis (Linnaeus): diffusion barriers, inorganic carbon limitation, and biochemical plasticity. J Exp Mar Biol Ecol 178:153–179CrossRefGoogle Scholar
  23. Muko S, Kawasaki K, Sakai K, Tasku F, Sigesada N (2000) Morphological plasticity in the coral Porites sillimani and its adaptive significance. Bull Mar Sci 66:225–239Google Scholar
  24. Nakamura Y, Shibuno T, Lecchini D, Kawamura T, Watanabe Y (2009) Spatial variability in habitat associations of pre- and post-settlement stages of coral reef fishes at Ishigaki Island, Japan. Mar Biol 156:2413–2419CrossRefGoogle Scholar
  25. Padilla-Gamino JL, Hanson KM, Stat M, Gates RD (2012) Phenotypic plasticity of the coral Porites rus: acclimatization responses to a turbid environment. J Exp Mar Biol Ecol 434:71–80CrossRefGoogle Scholar
  26. Pawlik JR, Steindler L, Henkel TP, Beer S, Ilan M (2007) Chemical warfare on coral reefs: sponge metabolites differentially affect coral symbiosis in situ. Limnol Oceanogr 52:907–911CrossRefGoogle Scholar
  27. Phillips NE, Shima JS (2010) Reproduction of the vermetid gastropod Dendropoma maximum (Sowerby, 1825) in Moorea, French Polynesia. J Molluscan Stud 76:133–137CrossRefGoogle Scholar
  28. Phillips NE, Shima JS, Osenberg CW (2014) Live coral cover may provide resilience to damage from the vermetid gastropod Dendropoma maximum by preventing larval settlement. Coral Reefs. doi: 10.1007/s00338-014-1198-2 CrossRefGoogle Scholar
  29. Rinkevich B, Loya Y (1985) Intraspecific competition in a reef coral: effects on growth and reproduction. Oecologia 66:100–105CrossRefGoogle Scholar
  30. River GF, Edmunds PJ (2001) Mechanisms of interaction between macroalgae and scleractinians on a coral reef in Jamaica. J Exp Mar Biol Ecol 261:159–172CrossRefGoogle Scholar
  31. Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:185–202CrossRefGoogle Scholar
  32. Sebens KP, Johnson TJ (1991) Effect of water movement on prey capture and distribution of reef corals. Hydrobiologia 226:91–101CrossRefGoogle Scholar
  33. Shima JS (1999) Variability in relative importance of determinants of reef fish recruitment. Ecol Lett 2:304–310CrossRefGoogle Scholar
  34. Shima JS (2001a) Recruitment of a coral reef fish: roles of settlement, habitat, and postsettlement losses. Ecology 82:2190–2199CrossRefGoogle Scholar
  35. Shima JS (2001b) Regulation of local populations of a coral reef fish via joint effects of density- and number-dependent mortality. Oecologia 126:58–65CrossRefGoogle Scholar
  36. Shima JS (2002) Mechanisms of density- and number-dependent population regulation of a coral-reef fish. Mar Fresh Res 53:175–179CrossRefGoogle Scholar
  37. Shima JS, Osenberg CW (2003) Cryptic density dependence: effects of spatio-temporal covariation between density and site quality in reef fish. Ecology 84:46–52CrossRefGoogle Scholar
  38. Shima JS, Osenberg CW, St Mary CM (2008) Quantifying site quality in a heterogeneous landscape: recruitment of a reef fish. Ecology 89:86–94CrossRefGoogle Scholar
  39. Shima JS, Osenberg CW, Stier AC (2010) The vermetid gastropod Dendropoma maximum reduces coral growth and survival. Biol Lett 6:815–818CrossRefGoogle Scholar
  40. Shima JS, Phillips NE, Osenberg CW (2013) Consistent deleterious effects of vermetid gastropods on coral performance. J Exp Mar Biol Ecol 439:1–6CrossRefGoogle Scholar
  41. Smith JE, Shaw M, Edwards RA, Obura D, Pantos O, Sala E, Sandin SA, Smriga S, Hatay M, Rohwer FL (2006) Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol Lett 9:835–845CrossRefGoogle Scholar
  42. Stier AC, McKeon CS, Osenberg CW, Shima JS (2010) Guard crabs alleviate deleterious effects of vermetid snails on a branching coral. Coral Reefs 29:1019–1022CrossRefGoogle Scholar
  43. Stimson J (2011) Ecological characterization of coral growth anomalies on Porites compressa in Hawai’i. Coral Reefs 30:133–142CrossRefGoogle Scholar
  44. Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337CrossRefGoogle Scholar
  45. Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  46. Wainwright SA, Koehl MAR (1976) The nature of flow and the reaction of benthic Cnidaria to it. In: Mackie GO (ed) Coelenterate ecology and behaviour. Plenum Press, New York, pp 5–21CrossRefGoogle Scholar
  47. Wielgus J, Glassom D, Ben-Shaprut O, Chadwick-Furman NE (2002) An aberrant growth form of Red Sea corals caused by polychaete infestations. Coral Reefs 21:315–316CrossRefGoogle Scholar
  48. 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 Berlin Heidelberg 2015

Authors and Affiliations

  • Jeffrey S. Shima
    • 1
  • Daniel McNaughtan
    • 1
  • Amanda T. Strong
    • 1
    • 2
  1. 1.School of Biological Sciences, and the Coastal Ecology LabUniversity of WellingtonVictoriaNew Zealand
  2. 2.Environmental Protection AuthorityWellingtonNew Zealand

Personalised recommendations