Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Turban snails as habitat for foliose algae: contrasting geographical patterns in species richness

Thomas Wernberg A B C G , Fernando Tuya C D E , Mads S. Thomsen C F and Gary A. Kendrick A
+ Author Affiliations
- Author Affiliations

A School of Plant Biology, University of Western Australia, Crawley, WA 6009, Australia.

B Australian Institute of Marine Science, Oceans Institute, Crawley, WA 6009, Australia.

C Centre for Marine Ecosystems Research, Edith Cowan University, Joondalup, WA 6027, Australia.

D CIIMAR, Rua dos Bragas, 289-4050-123, Porto, Portugal.

E BIOGES, Department of Biology, University of Las Palmas, Las Palmas 35010, Spain.

F Marine Department, National Environmental Research Institute, University of Aarhus, P.O. Box 4000, Roskilde, Denmark.

G Corresponding author. Email: thomas.wernberg@uwa.edu.au

Marine and Freshwater Research 61(11) 1237-1242 https://doi.org/10.1071/MF09184
Submitted: 20 July 2009  Accepted: 21 May 2010   Published: 16 November 2010

Abstract

Understanding patterns of species richness is a major goal for ecologists, especially in space-limited habitats where many organisms live on top of others (epibiosis, e.g. by algae growing on gastropods in marine environments). We tested the hypotheses that species richness of epiflora on the gastropod Turbo torquatus would not differ between regions with similarly rich algal floras, and that epifloral richness would increase with increasing gastropod size. Macroalgal floras of Hamelin Bay (HB), Marmion (M), Jurien Bay (JB) and Kalbarri (K), Western Australia, ranged from ~20 to 40 species reef–1 (JB = HB = M ≥ K). Epiflora on small T. torquatus (shell area <150 cm2) did not differ among regions but epifloral richness increased with increasing basibiont size. Large T. torquatus (>150 cm2) were only found in Hamelin Bay and Marmion, where epifloral richness differed substantially. Epifloral richness was positively related to basibiont size in Marmion but not in Hamelin Bay. However, densities of patellid limpets on large T. torquatus were ~4× higher in Hamelin Bay than in Marmion, implying that limpet grazing suppresses epifloral richness. Epifloral richness on turbinids is not simply associated with regional species pools or gastropod size; rather, biological interactions at the scale of individual basibionts apparently govern broad scale patterns of epibiosis.

Additional keywords: epibiosis, grazing, Turbinid snails, Turbo torquatus, Western Australia.


Acknowledgements

This research was supported by a Discovery grant from the Australian Research Council to T.W. and G.A.K. (DP0555929). M.S.T. was partially funded by the Danish Research Academy. We thank K. Cook for field assistance and D. Abdo for help with measuring Turbo surface areas. We also thank the Editor (A. Boulton), an Associate Editor, A. Davis, and an anonymous reviewer for comments that have improved the manuscript.


References

Abbott, L. L. , and Bergey, E. A. (2007). Why are there few algae on snail shells? The effects of grazing, nutrients and shell chemistry on the algae on shells of Helisoma trivolvis. Freshwater Biology 52, 2112–2120.
CrossRef |

Abdo, D. A. , Seager, J. W. , Harvey, E. S. , McDonald, J. I. , and Kendrick, G. A. , et al. (2006). Efficiently measuring complex sessile epibenthic organisms using a novel photogrammetric technique. Journal of Experimental Marine Biology and Ecology 339, 120–133.
CrossRef |

Bolton, J. J. (1994). Global seaweed diversity: patterns and anomalies. Botanica Marina 37, 241–246.
CrossRef |

Briggs, J. C. (2007). Marine biogeography and ecology: invasions and introductions. Journal of Biogeography 34, 193–198.
CrossRef |

Brown J. H. (1995). ‘Macroecology.’ (University of Chicago Press: Chicago.)

Buschbaum, C. , and Reise, K. (1999). Effects of barnacle epibionts on the periwinkle Littorina littorea (L.). Helgoland Marine Research 53, 56–61.
CrossRef |

Coleman, R. A. , Underwood, A. J. , Benedetti-Cecchi, L. , Aaberg, P. , and Arenas, F. , et al. (2006). A continental scale evaluation of the role of limpet grazing on rocky shores. Oecologia 147, 556–564.
CrossRef |

Connell, S. D. , and Irving, A. D. (2008). Integrating ecology with biogeography using landscape characteristics: a case study of subtidal habitat across continental Australia. Journal of Biogeography 35, 1608–1621.
CrossRef |

Connolly, S. R. , Menge, B. A. , and Roughgarden, J. (2001). A latitudinal gradient in recruitment of intertidal invertebrates in the northeast Pacific Ocean. Ecology 82, 1799–1813.
CrossRef |

Davis, A. R. , and White, G. A. (1994). Epibiosis in a guild of sessile subtidal invertebrates in south-eastern Australia: a quantitative survey. Journal of Experimental Marine Biology and Ecology 177, 1–14.
CrossRef |

Fletcher, W. J. (1987). Interactions among subtidal Australian sea urchins, gastropods and algae – effects of experimental removals. Ecological Monographs 57, 89–109.
CrossRef |

Foster, G. G. , and Hodgson, A. N. (2000). Intertidal population structure of the edible mollusc Turbo sarmaticus (Vetigastropoda) at an unexploited and exploited sites along the coast of the Eastern Cape Province, South Africa. African Zoology 35, 173–183.


Gilman, S. E. (2006). The northern geographic range limit of the intertidal limpet Collisella scabra: a test of performance, recruitment, and temperature hypotheses. Ecography 29, 709–720.
CrossRef |

Harman, N. , Harvey, E. S. , and Kendrick, G. A. (2003). Differences in fish assemblages from different reef habitats at Hamelin Bay, south-western Australia. Marine and Freshwater Research 54, 177–184.
CrossRef |

Irving, A. D. , and Connell, S. D. (2002). Sedimentation and light penetration interact to maintain heterogeneity of subtidal habitats: algal versus invertebrate dominated assemblages. Marine Ecology Progress Series 245, 83–91.
CrossRef |

Joll L. M. (1975). Reproduction and growth in two species of Turbinidae (Gastropoda Prosobranchia). M.Sc. thesis, University of Western Australia, Perth.

Keddy, P. A. (1992). Assembly and response rules two goals for predictive community ecology. Journal of Vegetation Science 3, 157–164.
CrossRef |

Kendrick, G. A. , Lavery, P. S. , and Philips, J. C. (1999). Influence of Ecklonia radiata kelp canopy structure on macro-algal assemblages in Marmion Lagoon, Western Australia. Hydrobiologia 399, 275–283.
CrossRef |

MacArthur R. H., and Wilson E. O. (1967). ‘The Theory of Island Biogeography.’ (Princeton University Press: Princeton.)

Pearce, C. M. , and Scheibling, R. E. (1990). Induction of metamorphosis of larvae of the green sea urchin, Strongylocentrotus droebachiensis, by coralline red algae. The Biological Bulletin 179, 304–311.
CrossRef |

Sala, E. , and Graham, M. H. (2002). Community-wide distribution of predator–prey interaction strength in kelp forests. Proceedings of the National Academy of Sciences of the United States of America 99, 3678–3683.
CrossRef |

Schmitt, R. J. , Osenberg, C. W. , and Bercovitch, M. G. (1983). Mechanisms and consequences of shell fouling in the kelp snail, Norrisia norrisi (Sowerby): indirect effects of octopus drilling. Journal of Experimental Marine Biology and Ecology 69, 267–281.
CrossRef |

Smale, D. A. , and Wernberg, T. (2009). Satellite-derived SST data as a proxy for water temperature in near-shore benthic ecology. Marine Ecology Progress Series 387, 27–37.
CrossRef |

Smale, D. A. , Kendrick, G. A. , and Wernberg, T. (2010). Assemblage turnover and taxonomic sufficiency of subtidal macroalgae at multiple spatial scales. Journal of Experimental Marine Biology and Ecology 384, 76–86.
CrossRef |

Thornber, C. (2007). Associational resistance mediates predator–prey interactions in a marine subtidal system. Marine Ecology (Berlin) 28, 480–486.
CrossRef |

Toohey, B. D. , Kendrick, G. A. , and Harvey, E. S. (2007). Disturbance and reef topography maintain high local diversity in Ecklonia radiata kelp forests. Oikos 116, 1618–1630.
CrossRef |

Tuya, F. , Wernberg, T. , and Thomsen, M. S. (2009a). Habitat structure affect abundances of labrid fishes across temperate reefs in south-western Australia. Environmental Biology of Fishes 86, 311–319.
CrossRef |

Tuya, F. , Wernberg, T. , and Thomsen, M. S. (2009b). Colonization of gastropods on subtidal reefs depends on density in adjacent habitats, not on disturbance regime. The Journal of Molluscan Studies 75, 27–33.
CrossRef |

Vanderklift, M. A. , and Kendrick, G. A. (2004). Variation in abundances of herbivorous invertebrates in temperate subtidal rocky reef habitats. Marine and Freshwater Research 55, 93–103.
CrossRef |

Vanderklift, M. A. , Lavery, P. S. , and Waddington, K. I. (2009). Intensity of herbivory on kelp by fish and sea urchins differs between inshore and offshore reefs. Marine Ecology Progress Series 376, 203–211.
CrossRef |

Wahl, M. (1989). Marine epibiosis. I. Fouling and antifouling: some basic aspects. Marine Ecology Progress Series 58, 175–189.
CrossRef |

Wahl, M. , and Mark, O. (1999). The predominantly facultative nature of epibiosis: experimental and observational evidence. Marine Ecology Progress Series 187, 59–66.
CrossRef |

Warner, G. F. (1997). Occurrence of epifauna on the periwinkle, Littorina littorea (L.), and interactions with the the polychaete Polydora ciliata (Johnston). Hydrobiologia 355, 41–47.
CrossRef |

Wernberg, T. , Kendrick, G. A. , and Phillips, J. C. (2003). Regional differences in kelp-associated algal assemblages on temperate limestone reefs in south-western Australia. Diversity & Distributions 9, 427–441.
CrossRef |

Wernberg, T. , White, M. , and Vanderklift, M. A. (2008). Population structure of turbinid gastropods on wave-exposed subtidal reefs: effects of density, body size and algae on grazing behaviour. Marine Ecology Progress Series 362, 169–179.
CrossRef |

Whittaker R. J., and Fernández-Palacios J. M. (2007). ‘Island Biogeography – Ecology, Evolution and Conservation.’ (Oxford University Press: London.)

Witman, J. D. , Etter, R. J. , and Smith, F. (2004). The relationship between regional and local species diversity in marine benthic communities: a global perspective. Proceedings of the National Academy of Sciences of the United States of America 101, 15 664–15 669.
CrossRef |



Rent Article (via Deepdyve) Export Citation Cited By (7)