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

Colour patterns in the sea urchin, Heliocidaris erythrogramma, suggest limited connectivity across the Southern and Pacific Ocean coastlines of Australia

Hayden J. Beck A and Craig A. Styan A B C
+ Author Affiliations
- Author Affiliations

A School of Life and Environmental Sciences, Deakin University, PO Box 423, Warrnambool, Vic. 3280, Australia. Present address: Environmental Geology Group, School of Geosciences, The University of Sydney, NSW 2006, Australia.

B Present address: RPS Environment, Level 2/47 Colin Street, West Perth, WA 6007, Australia and Oceans Institute, University of Western Australia, Stirling Highway, Crawley, WA 6009, Australia.

C Corresponding author. Email: Styanc@rpsgroup.com.au

Marine and Freshwater Research 61(2) 143-152 https://doi.org/10.1071/MF08156
Submitted: 17 May 2008  Accepted: 2 May 2009   Published: 25 February 2010

Abstract

Heliocidaris erythrogramma is a widespread Australian sea urchin whose colour varies greatly. Here we report large-scale, hierarchically structured surveys, testing for patterns in colouration of H. erythrogramma associated with wave exposure, and consistency between populations from the Pacific and Southern Oceans. Along the Southern Ocean coastline, more urchins with white dermis were found in (ocean swell-exposed) open coast regions, whereas more urchins with red dermis were usually found in the (ocean swell-protected) bay regions. In contrast, only red dermis urchins were found in both open coast and bay regions along the Pacific coastline. Spine colour was found to be independent of test colour within locations and, while no differences in the frequencies of spine colours were detected between regions of different wave exposure, differences were detected across 1–100s of km within coastlines. Large differences in the frequencies of spine colours were also detected between the two coastlines. Clear differences in two independent characteristics of colour between Southern Ocean and Pacific coastlines, combined with intermediate patterns at a location near the junction of these coastlines, suggest that large-scale morphological patterns might reflect intra-specific genetic differentiation within H. erythrogramma, large-scale environmental differences between temperate Australian coastlines, or an interaction between these two factors.

Additional keywords: hierarchical survey, morphology, polymorphism.


Acknowledgements

In total, 3412 urchins were collected (and then returned to the sea alive) with the help of Ryan Beck, Kevin Chisholm, Ben Dorner, Luke Dunlop, Matt Kuit, Doug Smith and Matt Wilson-Barnard. Funding for this work came from the Hermon Slade Foundation. Claire McClusky and two anonymous referees provided very useful comments on the manuscript. Samples were collected under scientific research permits from NSW and Victorian Department of Primary Industries. This study complies with the current laws of Australia.


References

Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.
CrossRef |

Anderson, M. J. , and Robinson, J. (2003). Generalized discriminant analysis based on distances. Australian and New Zealand Journal of Statistics 45, 301–318.
CrossRef |

Bandaranayake, W. M. (2006). The nature and role of pigments of marine invertebrates. Natural Product Reports 23, 223–255.
CrossRef | PubMed |

Beck H. J. (2007). Determining the pattern and cause of colour variation in the sea urchin Heliocidaris erythrogramma. B.Sc.(Honours) Thesis, Deakin University, Warrnambool, Victoria.

Clark, H. L. (1938). Echinoderms from Australia. Museum of Comparative Zoology (Harvard University). Memoirs 55, 404–406.


Constable A. J. (1989). Resource allocation in the sea urchin, Heliocidaris erythrogramma. Ph.D. Thesis, University of Melbourne.

Dalby, J. E. (1997a). Dimorphism in the ascidian Pyura stolonifera near Melbourne, Australia, and its evaluation through field transplant experiments. Marine Ecology 18, 253–271.
CrossRef |

Dalby, J. E. (1997b). Reproductive and electrophoretic evidence for genetic maintenance of dimorphism in the ascidian Pyura stolonifera near Melbourne, Australia. Ophelia 47, 227–243.


Dix, T. G. (1977). Reproduction in Tasmanian populations of Heliocidaris erythrogramma (Echinodermata: Echinometridae). Australian Journal of Marine and Freshwater Research 28, 509–520.
CrossRef |

Fowler-Walker, M. J. , Wernberg, T. , and Connell, S. D. (2006). Differences in kelp morphology between wave sheltered and exposed localities: morphologically plastic or fixed traits? Marine Biology 148, 755–767.
CrossRef |

Growns J. E. (1991). Some evolutionary and ecological implications of colour variation in the sea urchin Heliocidaris erythrogramma. Ph.D. Thesis, University of Tasmania, Hobart.

Growns, J. E. , and Ritz, D. A. (1994). Colour variation in southern Tasmania populations of Heliocidaris erythrogramma (Echinometridae: Echinoidea). Australian Journal of Marine and Freshwater Research 45, 233–242.
CrossRef |

Hidas, E. Z. , Costa, T. L. , Ayre, D. J. , and Minchinton, T. E. (2007). Is the species composition of rocky intertidal invertebrates across a biogeographic barrier in south-eastern Australia related to their potential for dispersal? Marine and Freshwater Research 58, 835–842.
CrossRef |

Kailola P. J., Williams M. J., Stewart P. C., Reichelt R. E., McNee A., and Grieve C. (1993). ‘Australian Fisheries Resources’. (Bureau of Resource Sciences and the Fisheries Research Corporation: Canberra.)

Keesing J. K. (2001). The ecology of Heliocidaris erythrogramma. In ‘Edible Sea Urchins: Biology and Ecology’. (Ed. J. M. Lawrence.) pp. 261–271. (Elsevier Science: Amsterdam.)

Levitan, D. R. (2002). The relationship between conspecific fertilization success and reproductive isolation among three congeneric sea urchins. Evolution 56, 1599–1609.
PubMed |

McMillan, W. O. , Raff, R. A. , and Palumbi, S. R. (1992). Population genetic consequences of developmental evolution in sea-urchins (Genus Heliocidaris). Evolution 46, 1299–1312.
CrossRef |

Metz, E. C. (1990). Rapid evolution of reproductive isolation by gamete incompatibility in Hawaiian sea urchins. Pacific Science 44, 192.


Millott, N. (1950). The sensitivity to light, reactions to shading, pigmentation, and color change of the sea urchin, Diadema antillarum Philippi. The Biological Bulletin 99, 329–330.
PubMed |

Miskelly A. (1968). ‘Sea Urchins of Australia and Indo-Pacific.’ (Capricorna Publications: Sydney.)

Mortensen T. (1943). ‘Monograph of Echinoidea. III, 3.’ (Reitzel: Copenhagen.)

O’Hara, T. D. , and Poore, G. C. B. (2000). Patterns of distribution for southern Australian marine echinoderms and decapods. Journal of Biogeography 27, 1321–1335.
CrossRef |

Rahman, S. M. , and Uehara, T. (2004). Interspecific and intraspecific variations in sibling species of sea urchin Echinometra. Comparative Biochemistry and Physiology 139, 469–478.
CrossRef |

Styan, C. A. (1997). Inexpensive and portable sampler for collecting eggs of free-spawning marine invertebrates underwater. Marine Ecology Progress Series 150, 293–296.
CrossRef |

Thomas I. M. (1982). Echinoderms (Phylum Echinodermata). In ‘Marine Invertebrates of Southern Australia Part I’. (Eds S. A. Shephard and I. M. Thomas.) pp. 395–476. (D.J. Woolman: Adelaide, Australia.)

Underwood A. J. (1997). ‘Ecological Experiments: their Logical Design and Interpretation using Analysis of Variance.’ (Cambridge University Press: Cambridge, UK.)

Underwood, A. J. , Chapman, M. G. , and Connell, S. D. (2000). Observations in ecology: you can’t make progress on processes without understanding the patterns. Journal of Experimental Marine Biology and Ecology 250, 97–115.
CrossRef | PubMed |

Valentine, J. P. , and Johnson, C. R. (2005). Persistence of sea urchin (Heliocidaris erythrogramma) barrens on the east coast of Tasmania: inhibition of macroalgal recovery in the absence of high densities of sea urchins. Botanica Marina 48, 106–115.
CrossRef |

Vanderklift, M. A. , and Kendrick, G. A. (2005). Variation in abundances of herbivorous invertebrates in temperate subtidal rocky reef habitats. Marine Ecology Progress Series 55, 93–103.


Waters, J. M. , and Roy, M. S. (2003). Marine biogeography of southern Australia: phylogeographical structure in a temperate sea-star. Journal of Biogeography 30, 1787–1796.
CrossRef |

Waters, J. M. , King, T. M. , O’Loughlin, P. M. , and Spencer, H. G. (2005). Phylogeographical disjunction in abundant high-dispersal littoral gastropods. Molecular Ecology 14, 2789–2802.
CrossRef | PubMed |

Waters, J. M. , McCulloch, G. A. , and Eason, J. A. (2007). Marine biogeographical structure in two highly dispersive gastropods: implications for trans-Tasman dispersal. Journal of Biogeography 34, 678–687.
CrossRef |

Wicksten, M. K. (1989). Why are there bright colours in sessile marine invertebrates? Bulletin of Marine Science 45, 519–530.


Williams, D. H. C. , and Anderson, D. T. (1975). Larval development and metamorphosis of the sea urchin Heliocidaris erythrogramma (Val.) (Echinoidea: Echinometridae). Australian Journal of Zoology 23, 371–403.
CrossRef |

Wright, J. T. , Dworjanyn, S. A. , Rogers, C. N. , and Steinberg, P. D. (2005). Density-dependent sea urchin grazing: differential removal of species, changes in community composition and alternative community states. Marine Ecology Progress Series 298, 143–156.
CrossRef |

Zigler, K. S. , Raff, E. C. , Popodi, P. , Raff, R. A. , and Lessios, H. A. (2003). Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57, 2293–2302.
PubMed |



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