Skip to main content
Log in

Two Pione species (Hadromerida, Clionaidae) from the Red Sea: a taxonomical challenge

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

Boring sponges of the genus Pione (Hadromerida, Clionaidae) are easily recognizable due to their spiculation. However, species identification is challenging, as the potentially diagnostic morphological character states of different species often overlap. For this reason, this group of species is frequently referred to as the ‘Pione vastifica complex’, after the most well-studied species of the genus. Boring-sponge samples were collected in the Red Sea and identified as P. cf. lampa and P. cf. vastifica, respectively. So far, these two species names have usually been considered as valid, although some authors suggested them to be synonymous. Morphological analyses were performed on spicules and micro-erosion patterns by means of both light and scanning electron microscopy. Two apparent morphotypes can be distinguished, mainly by the growth form, but statistical analysis does not support a clear separation in two species. In addition, a DNA barcoding approach using sequences of CO1 has not identified any nucleotide sequence differences. These data support the hypothesis that P. cf. lampa and P. cf. vastifica from the Red Sea are conspecific.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bierne, N., Bonhomme, F., & David, P. (2003). Habitat preference and the marine-speciation paradox. Proceedings of the Royal Society B, Biological Sciences, 270, 1399–1406.

    Article  PubMed  Google Scholar 

  • Calcinai, B., Cerrano, C., Sarà, M., & Bavestrello, G. (2000). Boring sponges (Porifera, Demospongiae) from the Indian Ocean. Italian Journal of Zoology, 67, 203–219.

    Article  Google Scholar 

  • Calcinai, B., Arillo, A., Cerrano, C., & Bavestrello, G. (2003). Taxonomy-related differences in the excavating micro-patterns of boring sponges. Journal of the Marine Biological Association of the United Kingdom, 83, 37–39.

    Google Scholar 

  • Carballo, J. L., Sanchez-Moyano, J. E., & Garcia-Gomez, J. C. (1994). Taxonomical and ecological remarks on boring sponges (Clionidae) from the Straits of Gibraltar (southern Spain): tentative bioindicators? Zoological Journal of the Linnean Society, 112, 407–424.

    Article  Google Scholar 

  • Carballo, J. L., Cruz-Barraza, J. A., & Gòmez, P. (2004). Taxonomy and description of clionaid sponges (Hadromerida, Clionaidae) from the Pacific Ocean of Mexico. Zoological Journal of the Linnean Society, 141, 353–397.

    Article  Google Scholar 

  • De Laubenfels, M. W. (1950). The Porifera of the Bermuda archipelago. Transactions of the Zoological Society of London, 27, 1–154. pls. I–II.

    Article  Google Scholar 

  • Desqueyroux-Faúndez, R. (1990). Spongiaires (Demospongiae) de l’Ile de Pâques (Isla de Pascua). Revue Suisse de Zoologie, 97, 373–409.

    Google Scholar 

  • Duran, S., & Rützler, K. (2006). Ecological speciation in a Caribbean marine sponge. Molecular Phylogenetics and Evolution, 40, 292–297.

    Article  CAS  PubMed  Google Scholar 

  • Duran, S., Pascual, M., & Turon, X. (2004). Low levels of genetic variation in mtDNA sequences over the western Mediterranean and Atlantic range of the sponge Crambe crambe (Poecilosclerida). Marine Biology, 144, 31–35.

    Article  CAS  Google Scholar 

  • Erpenbeck, D., Hooper, J. N. A., & Wörheide, G. (2006). CO1 phylogenies in diploblasts and the ‘Barcoding of Life’—are we sequencing a suboptimal partition? Molecular Ecology Notes, 6, 550–553.

    Article  CAS  Google Scholar 

  • Erpenbeck, D., Duran, S., Rützler, K., Paul, V., Hooper, J. N. A., & Wörheide, G. (2007). Towards a DNA taxonomy of Caribbean demosponges: a gene tree reconstructed from partial mitochondrial CO1 gene sequences supports previous rDNA phylogenies and provides a new perspective on the systematics of Demospongiae. Journal of the Marine Biological Association of the United Kingdom, 87, 1563–1570.

    CAS  Google Scholar 

  • Fromont, J., Craig, R., Rawlinson, L., & Alder, J. (2005). Excavating sponges that are destructive to farmed pearl oysters in Western and Northern Australia. Aquaculture Research, 36, 150–162.

    Article  Google Scholar 

  • Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4, 1–9.

    Google Scholar 

  • Hancock, A. (1849). On the excavating powers of certain sponges belonging to the genus Cliona with descriptions of several new species, and an allied generic form. Annals and Magazine of Natural History. 2nd Series, 3, 321–348. pls. XII–XV.

    Google Scholar 

  • Huelsenbeck, J. P., & Ranala, B. (2004). Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology, 53, 904–913.

    Article  PubMed  Google Scholar 

  • Jory, D. E., & Iversen, E. S. (1985). Molluscan mariculture in the Greater Caribbean: an overview. Marine Fisheries Review, 47, 1–10.

    Google Scholar 

  • Klautau, M., Russo, C. A. M., Lazoski, C., Boury-Esnault, N., Thorpe, J. P., & Sole-Cava, A. M. (1999). Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution, 53, 1414–1422.

    Article  Google Scholar 

  • Lazoski, C., Solè-Cava, A. M., Boury-Esnault, N., Klautau, M., & Russo, C. A. M. (2001). Cryptic speciation in a high gene flow scenario in the oviparous marine sponge Chondrosia reniformis. Marine Biology, 139, 421–429.

    Article  CAS  Google Scholar 

  • Maddison, W. P., & Maddison, D. R. (1992). MacClade: Analysis of phylogeny and character evolution. Sunderland: Sinauer Associates.

    Google Scholar 

  • Mariani, S., Uriz, M. J., & Turon, X. (2000). Larval bloom of the oviparous sponge Cliona viridis: coupling of larval abundance and adult distribution. Marine Biology, 137, 783–790.

    Article  Google Scholar 

  • McKenna, S. A. (1997). Interactions between the boring sponge, Cliona lampa and two hermatypic corals from Bermuda. Proceedings of the 8th International Coral Reef Symposium, 2, 1369–1374.

    Google Scholar 

  • Meyer, C. P., Geller, J. B., & Paulay, G. (2005). Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evolution, 59, 113–125.

    PubMed  Google Scholar 

  • Nichols, S. A., & Barnes, P. A. G. (2005). A molecular phylogeny and historical biogeography of the marine sponge genus Placospongia (Phylum Porifera) indicate low dispersal capabilities and widespread crypsis. Journal of Experimental Marine Biology and Ecology, 323, 1–15.

    Article  Google Scholar 

  • Palumbi, S. R., Grabowsky, G., Duda, T., Geyer, L., & Tachino, N. (1997). Speciation and population genetic structure in tropical Pacific Sea urchins. Evolution, 51, 1506–1517.

    Article  Google Scholar 

  • Pang, R. K. (1973). The systematics of some Jamaican excavating sponges (Porifera). Postilla, 161, 1–75.

    Google Scholar 

  • Posada, D., & Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

    Article  CAS  PubMed  Google Scholar 

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  • Rosell, D. (1994). Morphological and ecological relationships of two clionid sponges. Ophelia, 40, 37–50.

    Google Scholar 

  • Rosell, D., & Uriz, M. J. (1997). Phylogenetic relationships within the excavating Hadromerida (Porifera), with a systematic revision. Cladistics, 13, 349–366.

    Article  Google Scholar 

  • Rosell, D., & Uriz, M. J. (2002). Excavating and endolithic sponge species (Porifera) from the Mediterranean: species descriptions and identification key. Organisms Diversity and Evolution, 2, 55–86.

    Article  Google Scholar 

  • Rützler, K. (1973). Clionid sponges from the coast of Tunisia. Bulletin de l’Institut d’Océanographie et de Peche, Salammbo, 2, 623–636.

    Google Scholar 

  • Rützler, K. (1974). The burrowing sponges of Bermuda. Smithsonian Contributions to Zoology, 165, 1–32.

    Google Scholar 

  • Rützler, K. (2002a). Family Clionaidae D’Orbigny, 1851. In J. N. A. Hooper & R. W. M. Van Soest (Eds.), Systema Porifera: A guide to the classification of sponges (pp. 173–185). New York: Kluger Academic/Plenum.

    Google Scholar 

  • Rützler, K. (2002b). Impact of crustose clionid sponges on Caribbean reef corals. Acta Geologica Hispanica, 37, 61–72.

    Google Scholar 

  • Rützler, K., & Stone, S. M. (1986). Discovery and significance of Albany Hancock’s microscope preparations of excavating sponges (Porifera: Hadromerida: Clionidae). Proceedings of the Biological Society of Washington, 99, 659–675.

    Google Scholar 

  • Schönberg, C. H. L. (2002). Pione lampa, a bioeroding sponge in a worm reef. Hydrobiologia, 482, 49–68.

    Article  Google Scholar 

  • Schönberg, C. H. L., & Beuck, L. (2007). Where Topsent went wrong: Aka infesta a.k.a. Aka labyrinthica (Demospongiae: Phloeodictyidae) and implications for other Aka spp. Journal of the Marine Biological Association of the United Kingdom, 87, 1459–1476.

    Article  Google Scholar 

  • Van Soest, R. W. M, Boury-Esnault, N., Hooper, J. N. A., Rützler, K, de Voogd, N. J., Alvarez, B., et al. (2008). World Porifera database. http://www.marinespecies.org/porifera. Accessed 12 March 2009.

  • Wörheide, G. (2006). Low variation in partial cytochrome oxidase subunit I (COI) mitochondrial sequences in the coralline demosponge Astrosclera willeyana across the Indo-Pacific. Marine Biology, 148, 907–912.

    Article  Google Scholar 

  • Zundelevich, A., Lazar, B., & Ilan, M. (2007). Chemical versus mechanical bioerosion of coral reefs by boring sponges—lessons from Pione cf. vastifica. Journal of Experimental Biology, 210, 91–96.

    Article  CAS  PubMed  Google Scholar 

  • Zwickl, D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation. Austin, Texas: University of Texas at Austin.

Download references

Acknowledgements

Thanks are due to Dr. Francesca Benzoni, Bicocca University, Milano, who provided international contacts. We also thank Dr. Rady Talaat, Dr. Mohammed Salem and Dr. Yasser Awadalla at the Training Center of the Egyptian Environmental Affairs Agency in Sharm el Sheik for their hospitality, and Dr. Fouda of the Egyptian Environmental Affairs Agency, Nature Conservation Sector, for field work permission. Further thanks are due to Judith Pöppe, who helped with the molecular analysis. We are also grateful to Christine Hanna Lydia Schönberg and Shimrit Perkol-Finkel for their comments, to Massimo Ponti and Giovanni Fontana, Bologna University, and to Mario Mori, Università Politecnica delle Marche, for helping with statistical analysis and image editing. Thanks are due to the referees for their the critical comments, which have greatly improved the quality of the manuscript. Special thanks go to Maria Luisa Zanzottera and Erasmo Ferrario.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Filippo Ferrario.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ferrario, F., Calcinai, B., Erpenbeck, D. et al. Two Pione species (Hadromerida, Clionaidae) from the Red Sea: a taxonomical challenge. Org Divers Evol 10, 275–285 (2010). https://doi.org/10.1007/s13127-010-0027-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-010-0027-x

Keywords

Navigation