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Hydrobiologia

, Volume 687, Issue 1, pp 205–217 | Cite as

Phenotypic variability in the Caribbean Orange Icing sponge Mycale laevis (Demospongiae: Poecilosclerida)

  • Tse-Lynn Loh
  • Susanna López-Legentil
  • Bongkeun Song
  • Joseph R. Pawlik
SPONGE RESEARCH DEVELOPMENTS

Abstract

Sponge species may present several morphotypes, but sponges that are morphologically similar can be separate species. We investigated morphological variation in Mycale laevis, a common Caribbean reef sponge. Four morphotypes of M. laevis have been observed (1) orange, semi-cryptic, (2) orange, massive, (3) white, semi-cryptic, and (4) white, massive. Samples of M. laevis were collected from Key Largo, Florida, the Bahamas Islands, and Bocas del Toro, Panama. Fragments of the 18S and 28S rRNA ribosomal genes were sequenced and subjected to phylogentic analyses together with sequences obtained for 11 other Mycale species and additional sequences retrieved from GenBank. Phylogenetic analyses confirmed that the genus Mycale is monophyletic within the Order Poecilosclerida, although the subgenus Aegogropila is polyphyletic and the subgenus Mycale is paraphyletic. All 4 morphotypes formed a monophyletic group within Mycale, and no genetic differences were observed among them. Spicule lengths did not differ among the 4 morphotypes, but the dominant megasclere in samples collected from Florida and the Bahamas was the strongyle, while those from Panama had subtylostyles. Our data suggest that the 4 morphotypes constitute a single species, but further studies would be necessary to determine whether skeletal variability is due to phentotypic or genotypic plasticity.

Keywords

Porifera 18S rRNA 28S rRNA Ribosomal DNA Caribbean Morphotype Genotype 

Notes

Acknowledgments

This research was funded by the National Science Foundation (OCE-0550468, 1029515), NOAA/NURC (NA96RU-0260) and NOAA’s Coral Reef Conservation Program with additional support from the UNCW Brauer Fellowship, the AMNH Lerner-Gray Fund, and the Spanish Government project CTM2010-17755. Sponge collection in Florida was carried out under permit number FKNMS-2007-034. The authors would like to thank members of the Pawlik and Song laboratories, staff of STRI Bocas, crew of R/V Walton-Smith and R/V Cape Hatteras, Z. Jaafar, and J. Vicente for laboratory and field assistance. W. Freshwater helped with phylogenetic analyses. Molecular work was carried out at the UNCW Center for Marine Science DNA Core Facility.

References

  1. Blanquer, A. & M. J. Uriz, 2007. Cryptic speciation in marine sponges evidenced by mitochondrial and nuclear genes: a phylogenetic approach. Molecular Phylogenetics and Evolution 45: 392–397.PubMedCrossRefGoogle Scholar
  2. Blanquer, A., M. J. Uriz & G. Agell, 2008. Hidden diversity in sympatric sponges: adjusting life-history dynamics to share substrate. Marine Ecology Progress Series 371: 109–115.CrossRefGoogle Scholar
  3. Chapman, M. G., T. J. Tolhurst, R. J. Murphy & A. J. Underwood, 2010. Complex and inconsistent patterns of variation in benthos, micro-algae and sediment over multiple spatial scales. Marine Ecology Progress Series 398: 33–47.CrossRefGoogle Scholar
  4. Chou, L. M., J. Y. Yu & T. L. Loh, 2004. Impacts of sedimentation on soft-bottom benthic communities in the southern islands of Singapore. Hydrobiologia 515: 91–106.CrossRefGoogle Scholar
  5. Collin, R., M. C. Diaz, J. L. Norenburg, R. M. Rocha, J. A. Sanchez, A. Schulze, M. Schwartz & A. Valdez, 2005. Photographic identification guide to some common marine invertebrates of Bocas Del Toro, Panama. Caribbean Journal of Science 41: 638–707.Google Scholar
  6. Corredor, J. E., C. R. Wilkinson, V. P. Vicente, J. M. Morell & E. Otero, 1988. Nitrate release by Caribbean reef sponges. Limnology and Oceanography 33: 114–120.CrossRefGoogle Scholar
  7. Diaz, M. C. & K. Rutzler, 2001. Sponges: an essential component of Caribbean coral reefs. Bulletin of Marine Science 69: 535–546.Google Scholar
  8. Duran, S. & K. Rützler, 2006. Ecological speciation in a Caribbean marine sponge. Molecular Phylogenetics and Evolution 40: 292–297.PubMedCrossRefGoogle Scholar
  9. Erpenbeck, D., S. Duran, K. Rützler, V. Paul, J. N. A. Hooper & G. Wörheide, 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.Google Scholar
  10. Goreau, T. F. & W. D. Hartman, 1966. Sponge: effect on the form of reef corals. Science 151: 343–344.PubMedCrossRefGoogle Scholar
  11. Guindon, S. & O. Gascuel, 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696–704.PubMedCrossRefGoogle Scholar
  12. Hajdu, E. & K. Rutzler, 1998. Sponges, genus Mycale (Poecilosclerida: Demospongiae: Porifera), from a Caribbean mangrove and comments on subgeneric classification. Proceedings of the Biological Society of Washington 111: 737–773.Google Scholar
  13. Hartman, W. D., 1967. Revision of Neofibularia (Porifera, Demospongiae), a genus of toxic sponges from the West Indies and Australia. Postilla 113: 1–41.Google Scholar
  14. Henkel, T. P. & J. R. Pawlik, 2005. Habitat use by sponge-dwelling brittlestars. Marine Biology 146: 301–313.CrossRefGoogle Scholar
  15. Hill, M. S., 1998. Spongivory on Caribbean reefs releases corals from competition with sponges. Oecologia 117: 143–150.CrossRefGoogle Scholar
  16. Hooper, J., 1985. Character stability, systematic, and affinities between Microcionidae (Poecilosclerida) and Axinellida. In Rützler, K. (ed.), New Perspectives in Sponge Biology. Smithsonian Institution Press, Washington: 284–294.Google Scholar
  17. Hooper, J. N. A. & R. Van Soest, 2002. Systema Porifera: A Guide to the Classification of Sponges, Vol. 1. Kluwer Academic, New York.Google Scholar
  18. Klautau, M., C. A. M. Russo, C. Lazoski, N. Boury-Esnault, J. P. Thorpe & A. M. Solé-Cava, 1999. Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53: 1414–1422.CrossRefGoogle Scholar
  19. Loh, T.-L. & J. R. Pawlik, 2009. Bitten down to size: fish predation determines growth form of the Caribbean coral reef sponge Mycale laevis. Journal of Experimental Marine Biology and Ecology 374: 45–50.CrossRefGoogle Scholar
  20. López-Legentil, S., P. M. Erwin, T. P. Henkel, T. -L. Loh & J. P. Pawlik, 2010. Phenotypic plasticity in the Caribbean sponge Callyspongia vaginalis (Porifera: Haplosclerida). Scientia Marina 74: 445–453.CrossRefGoogle Scholar
  21. Maldonado, M., M. Carmona & M. Uriz, 1999. Decline in Mesozoic reef-building sponges explained by silicon limitation. Nature 401: 785–788.CrossRefGoogle Scholar
  22. McDonald, J. I., J. N. A. Hooper & K. A. McGuinness, 2002. Environmentally influenced variability in the morphology of Cinachyrella australiensis (Carter 1886) (Porifera: Spirophorida: Tetillidae). Marine and Freshwater Research 53: 79–84.CrossRefGoogle Scholar
  23. Micheli, F., L. Benedetti-Cecchi, S. Gambaccini, I. Bertocci, C. Borsini, G. C. Osio & F. Romano, 2005. Cascading human impacts, marine protected areas, and the structure of Mediterranean reef assemblages. Ecological Monographs 75: 81–102.CrossRefGoogle Scholar
  24. Miller, K., B. Alvarez, C. Battershill & P. Northcote, 2001. Genetic, morphological, and chemical divergence in the sponge genus Latrunculia (Porifera: Demospongiae) from New Zealand. Marine Biology 139: 235–250.CrossRefGoogle Scholar
  25. Palumbi, S. R., 1986. How body plans limit acclimation: responses of a demosponge to wave force. Ecology 67: 208–214.CrossRefGoogle Scholar
  26. Pawlik, J. R., B. Chanas, R. J. Toonen & W. Fenical, 1995. Defenses of Caribbean sponges against predatory reef fish: I. Chemical deterrence. Marine Ecology Progress Series 127: 183–194.CrossRefGoogle Scholar
  27. Pile, A. J., M. R. Patterson & J. D. Witman, 1996. In situ grazing on plankton <10 μm by the boreal sponge Mycale lingua. Marine Ecology Progress Series 141: 95–102.CrossRefGoogle Scholar
  28. Posada, D., 2003. Using Modeltest and PAUP* to select a model of nucleotide substitution. In Baxevanis, A. D. D. B. Davison, R. D. M. Page, G. A. Petsko, L. D. Stein, & G. D. Stormo (eds), Current Protocols in Bioinformatics. Wiley, New York: 6.5.1–6.5.14.Google Scholar
  29. Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.PubMedCrossRefGoogle Scholar
  30. Randall, J. & W. Hartman, 1968. Sponge-feeding fishes of the West Indies. Marine Biology 1: 216–225.CrossRefGoogle Scholar
  31. Ronquist, F. & J. P. Huelsenbeck, 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.PubMedCrossRefGoogle Scholar
  32. Rozas, J., J. C. Sanchez-DelBarrio, X. Messeguer & R. Rozas, 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496–2497.PubMedCrossRefGoogle Scholar
  33. Schneider, S., D. Roessli & L. Excoffier, 2000. Arlequin ver. 2000. A software for population genetics data analysis. Genetics and Biometry Laboratory, Department of Anthropology, University of Geneva, Geneva.Google Scholar
  34. Sollas, I., 1908. The inclusion of foreign bodies by sponges, with a description of a new genus and species of Monaxonida. Annals & Magazine of Natural History 1: 395–401.CrossRefGoogle Scholar
  35. Southwell, M. W., J. B. Weisz, C. S. Martens & N. Lindquist, 2008. In situ fluxes of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida. Limnology and Oceanography 53: 986–996.CrossRefGoogle Scholar
  36. Swofford, D. L., 1998. PAUP*4.0, version b10. Sinuaer, Sunderland, MA.Google Scholar
  37. Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology & Evolution 10: 512–526.Google Scholar
  38. Tamura, K., J. Dudley, M. Nei & S. Kumar, 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology & Evolution 24: 1596–1599.CrossRefGoogle Scholar
  39. Teragawa, C. K., 1986. Particle transport and incorporation during skeleton formation in a keratose sponge: Dysidea etheria. Biological Bulletin 170: 321–334.CrossRefGoogle Scholar
  40. Van Soest, R. M., 1984. Marine sponges from Curacao and other Caribbean localities. Part III Poecilosclerida. In Hummelinck, P. W. & L. J. Van Der Steen (eds), Studies on the Fauna of Curacao and Other Caribbean Islands No. 199. Foundation for Scientific Research in Surinam and the Netherland Antilles, Utrecht: 1–187.Google Scholar
  41. Wilkinson, C., 2008. Status of Coral Reefs of the World: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre. Townsville, Australia.Google Scholar
  42. Williams, E. H. & L. Bunkley-Williams, 1990. The worldwide coral reef bleaching cycle and related sources of coral mortality. Atoll Research Bulletin 335: 1–71.Google Scholar
  43. Wulff, J. L., 1997. Parrotfish predation on cryptic sponges of Caribbean coral reefs. Marine Biology 129: 41–52.CrossRefGoogle Scholar
  44. Wulff, J. L., 2006a. Rapid diversity and abundance decline in a Caribbean coral reef sponge community. Biological Conservation 127: 167–176.CrossRefGoogle Scholar
  45. Wulff, J. L., 2006b. Sponge systematics by starfish: Predators distinguish cryptic sympatric species of Caribbean Fire Sponges, Tedania ignis and Tedania klausi n. sp. (Demospongiae, Poecilosclerida). Biological Bulletin 211: 83–94.PubMedCrossRefGoogle Scholar
  46. Zea, S., 1987. Esponjas del Caribe Colombiano, 1st ed. Catalogo Cientifico, Bogotá.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Tse-Lynn Loh
    • 1
  • Susanna López-Legentil
    • 2
  • Bongkeun Song
    • 1
  • Joseph R. Pawlik
    • 1
  1. 1.Center for Marine ScienceUniversity of North Carolina WilmingtonWilmingtonUSA
  2. 2.Department of Animal Biology (Invertebrates)University of BarcelonaBarcelonaSpain

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