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Impacts of Hurricanes Irma and Maria on Coral Reef Sponge Communities in St. Thomas, U.S. Virgin Islands

  • Deborah J. GochfeldEmail author
  • Julie B. Olson
  • Andia Chaves-Fonnegra
  • Tyler B. Smith
  • Rosmin S. Ennis
  • Marilyn E. Brandt
Special Issue: Impact of 2017 Hurricanes

Abstract

Many studies have evaluated the impacts of hurricanes on coral communities, but far less is known about impacts, recovery, and resilience of sponge communities to these extreme events. In September 2017, St. Thomas, U.S. Virgin Islands, was impacted by two Category 5 hurricanes within 2 weeks: Hurricanes Irma and Maria. Such extreme events occurring in such rapid succession are virtually unprecedented. Pre-hurricane (2015, 2016) surveys of permanent transects at six sites around St. Thomas were compared with those at 10 weeks post-hurricanes (December 2017) to evaluate storm impacts on sponges and on benthic coral reef constituents. These surveys also established a baseline for evaluating future recovery. Percent cover of sponges declined by 24.9% post-hurricanes. In contrast, sponge density increased by 43.9% from 2015 to 2016 and declined slightly after the hurricanes. Overall sponge volume did not vary over time, and whereas sponge diversity was similar in 2015 and 2016, it increased post-hurricanes. Sponge morphologies were differentially affected by the hurricanes; the proportion of upright sponges declined by 36.9%, while there was a 24.4% increase in encrusting sponges. Coral and macroalgal cover did not change significantly over the sampling period, while percent cover of epilithic algae increased and non-living substrata decreased from 2015 to 2016 but did not change further post-hurricanes. At all sites, recruitment and/or regrowth of sponges was observed within 10 weeks post-hurricanes, indicating potential resilience in Caribbean sponge communities. Whether these sponge communities return to pre-hurricane conditions and how long that will take remains to be seen.

Keywords

Hurricane impacts Sponge community Coral reef community Sponge morphology U.S. Virgin Islands 

Notes

Acknowledgments

We thank A. Gutting and L. Olinger for their help in the field, M. Slattery for his comments on the manuscript, and the Captain and crew of the R/V F.G. Walton Smith. Research was conducted under Virgin Islands Department of Planning and Natural Resources permits DFW15085T and DFW17039T. This is contribution no. 201 from the University of the Virgin Islands’ Center for Marine and Environmental Studies.

Funding information

Funding was provided by a National Oceanic and Atmospheric Administration Coral Reef Conservation Program grant (no. NA15NOS4820074) to ME Brandt, DJ Gochfeld, and JB Olson and by National Science Foundation RAPID Collaborative grants (nos. OCE-1807807, OCE-1808233, and OCE-1810616) to DJ Gochfeld, JB Olson, and ME Brandt, respectively.

Supplementary material

12237_2020_694_MOESM1_ESM.pdf (3.7 mb)
ESM 1 (PDF 3821 kb)

References

  1. Alvarez-Filip, L., and I. Gil. 2006. Effects of Hurricanes Emily and Wilma on coral reefs in Cozumel, Mexico. Coral Reefs 25: 583.CrossRefGoogle Scholar
  2. Anthony, Kenneth R.N., Jeffrey A. Maynard, Guillermo Diaz-Pulido, Peter J. Mumby, Paul A. Marxhall, Long Cao, and Ove Hoegh-Guldberg. 2011. Ocean acidification and warming will lower coral reef resilience. Global Change Biology 17: 1798–1808.  https://doi.org/10.1111/j.1365-2486.2010.02364.x.CrossRefGoogle Scholar
  3. Aranceta-Garza, F., E.F. Balart, H. Reyes-Bonilla, and P. Cruz-Hernández. 2012. Effect of tropical storms on sexual and asexual reproduction in coral Pocillopora verrucosa subpopulations in the Gulf of California. Coral Reefs 31: 1157–1167.CrossRefGoogle Scholar
  4. Arias-Gonzalez, Jesús Ernesto, Tak Fung, Robert M. Seymour, Joaquín Rodrigo Garza-Pérez, Gilberto Acosta-González, Yves-Marie Bozec, and Craig R. Johnson. 2017. A coral-algal phase shift in Mesoamerica not driven by changes in herbivorous fish abundance. PLoS One 12 (4): e0174855.  https://doi.org/10.1371/journal.pone.0174855.CrossRefGoogle Scholar
  5. Aronson, R.B., W.F. Precht, M.A. Toscano, and K.H. Koltes. 2002. The 1998 bleaching event and its aftermath on a coral reef in Belize. Marine Biology 141: 435–447.CrossRefGoogle Scholar
  6. Bates, Douglas, Martin Mächler, Benjamin M. Bolker, and Steven C. Walker. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.  https://doi.org/10.18637/jss.v067.i01.
  7. Bell, James J. 2008. The functional roles of marine sponges. Estuarine, Coastal and Shelf Science 79: 341–353.CrossRefGoogle Scholar
  8. Bell, James J., Simon K. Davy, Timothy Jones, Michael W. Taylor, and Nicole S. Webster. 2013. Could some coral reefs become sponge reefs as our climate changes? Global Change Biology 19 (9): 2613–2624.CrossRefGoogle Scholar
  9. Bell, James J., Megan Shaffer, Holly Bennett, Emily McGrath, Charli Mortimer, Alberto Rovellini, Joseph Marlow, Andrew Biggerstaff, and José Luis Carballo. 2017a. Impacts of short-term large-scale climatic variation on sponge assemblages. In Climate change, ocean acidification and sponges, ed. José Luis Carballo and James J. Bell, 143–177. Cham: Springer International.CrossRefGoogle Scholar
  10. Bell, James J., Andrew Biggerstaff, Tracey Bates, Holly Bennett, Joseph Marlow, Emily McGrath, and Megan Shaffer. 2017b. Sponge monitoring: Moving beyond diversity and abundance. Ecological Indicators 78: 470–488.CrossRefGoogle Scholar
  11. Bell, James J., Alberto Rovellini, Simon K. Davy, Michael W. Taylor, Elizabeth A. Fulton, Matthew R. Dunn, Holly M. Bennett, Nora M. Kandler, Heidi M. Luter, and Nicole S. Webster. 2018. Climate change alterations to ecosystem dominance: How might sponge-dominated reefs function? Ecology 99 (9): 1920–1931.CrossRefGoogle Scholar
  12. Biggerstaff, A., J. Jompa, and J.J. Bell. 2017. Increasing benthic dominance of the phototrophic sponge Lamellodysidea herbacea on a sedimented reef within the Coral Triangle. Marine Biology 164 (12): 220–216.  https://doi.org/10.1007/s00227-017-3253-3.CrossRefGoogle Scholar
  13. Biggs, Brendan C. 2013. Harnessing natural recovery processes to improve restoration outcomes: An experimental assessment of sponge-mediated coral reef restoration. PLoS One 8 (6): e64945.  https://doi.org/10.1371/journal.pone.0064945.CrossRefGoogle Scholar
  14. Blair, Stephen M., Timothy L. McIntosh, and Benjamin J. Mostkoff. 1994. Impacts of Hurricane Andrew on the offshore reef systems of central and northern Dade County, Florida. Bulletin of Marine Science 54: 961–973.Google Scholar
  15. Brandt, Marilyn E., Lauren K. Olinger, Andia Chaves-Fonnegra, Julie B. Olson, and Deborah J. Gochfeld. 2019. Coral recruitment is impacted by the presence of a sponge community. Marine Biology 166 (4): 49–13.  https://doi.org/10.1007/s00227-019-3493-5.CrossRefGoogle Scholar
  16. Camp, Joanne, Adam A. Scaife, and Julian Heming. 2018. Predictability of the 2017 North Atlantic hurricane season. Atmospheric Science Letters 2018: 19e813.  https://doi.org/10.1002/asl.813.CrossRefGoogle Scholar
  17. Cangialosi, John P., Andrew S. Latto, and Robbie Berg. 2018. Hurricane Irma (AL112017). National Hurricane Center Tropical Cyclone Report. 111 pp.
  18. Chaves-Fonnegra, Andia, Kevin A. Feldheim, Jesse Secord, and Jose V. Lopez. 2015. Population structure and dispersal of the coral-excavating sponge Cliona delitrix. Molecular Ecology 24 (7): 1447–1466.CrossRefGoogle Scholar
  19. Chaves-Fonnegra, Andia, Manuel Maldonado, Patricia Blackwelder, and Jose V. Lopez. 2016. Asynchronous reproduction and multi-spawning in the coral-excavating sponge Cliona delitrix. Journal of the Marine Biological Association of the United Kingdom 96: 515–528.CrossRefGoogle Scholar
  20. Chaves-Fonnegra, Andia, Behrnard Riegl, Sven Zea, Jose V. Lopez, Tyler Smith, Marilyn Brandt, and David S. Gilliam. 2018. Bleaching events regulate shifts from corals to excavating sponges in algae-dominated reefs. Global Change Biology 24: 773–785.CrossRefGoogle Scholar
  21. Clarke, K.R., and R.M. Warwick. 2001. Change in marine communities: An approach to statistical analysis and interpretation. 2nd ed. Plymouth: PRIMER-E.Google Scholar
  22. Coffroth, Mary Alice, and Howard R. Lasker. 1998. Population structure of a clonal gorgonian coral: The interplay between clonal reproduction and disturbance. Evolution 52 (2): 379–393.CrossRefGoogle Scholar
  23. Cropper, Wendell P., Jr., and Daniel DiResta. 1999. Simulation of a Biscayne Bay, Florida commercial sponge population: Effects of harvesting after Hurricane Andrew. Ecological Modelling 118: 1–15.CrossRefGoogle Scholar
  24. de Goeij, M. Jasper, Dick van Oevelen, Mark J.A. Vermeij, Ronaled Osinga, Jack J. Middleburg, Anton F.P.M. de Goeij, and Wim Admiraal. 2013. Surviving in a marine desert: The sponge loop retains resources within coral reefs. Science 342 (6154): 108–110.CrossRefGoogle Scholar
  25. De’ath, Glenn, Katharina E. Fabricius, Hugh Sweatman, and Marji Puotinen. 2012. The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences 109 (44): 17995–17999.  https://doi.org/10.1073/pnas.1208909109.CrossRefGoogle Scholar
  26. DeBiasse, M.B., V.P. Richards, and M.S. Shivji. 2010. Genetic assessment of connectivity in the common reef sponge, Callyspongia vaginalis (Demospongiae: Haplosclerida) reveals high population structure along the Florida reef tract. Coral Reefs 29: 47–55.CrossRefGoogle Scholar
  27. Diaz, M. Cristina, and Klaus Rützler. 2001. Sponges: An essential component of Caribbean coral reefs. Bulletin of Marine Science 69: 535–546.Google Scholar
  28. Diaz, Maria Cristina, and Klaus Rützler. 2011. Biodiversity of sponges: Belize and beyond, to the greater Caribbean. In Too precious to drill: The marine biodiversity of Belize, ed. Mariea Lourdes D. Palomares and Daniel Pauly, 57–65. Fisheries Centre Research Reports 19(6). Vancouver: Fisheries Centre, University of British Columbia.Google Scholar
  29. Dudgeon, Steve R., Richard B. Aronson, John F. Bruno, and William F. Precht. 2010. Phase shifts and stable states on coral reefs. Marine Ecology Progress Series 413: 201–216.CrossRefGoogle Scholar
  30. Easson, Cole G., Marc Slattery, Henrique G. Momm, Julie B. Olson, Robert W. Thacker, and Deborah J. Gochfeld. 2013. Exploring individual- to population-level impacts of disease on coral reef sponges: Using spatial analysis to assess the fate, dynamics, and transmission of Aplysina red band syndrome (ARBS). PLoS One 8 (11): e79976.  https://doi.org/10.1371/journal.pone.0079976.CrossRefGoogle Scholar
  31. Easson, Cole G., Kenan O. Matterson, Christopher J. Freeman, Stephanie K. Archer, and Robert W. Thacker. 2015. Variation in species diversity and functional traits of sponge communities near human populations in Bocas del Toro, Panama. Peer J 3: e1385.  https://doi.org/10.7717/peerj.1385.CrossRefGoogle Scholar
  32. Edmunds, Peter J. 2019. Three decades of degradation lead to diminished impacts of severe hurricanes on Caribbean reefs. Ecology 100 (3): e02587.  https://doi.org/10.1002/ecy.2587.CrossRefGoogle Scholar
  33. Edmunds, Peter J., and Jon D. Witman. 1991. Effect of Hurricane Hugo on the primary framework of a reef along the south shore of St. John, US Virgin Islands. Marine Ecology Progress Series 78: 201–204.CrossRefGoogle Scholar
  34. Edmunds, Peter J., Georgios Tsounis, Ralf Boulon, and Lorenzo Bramanti. 2019. Acute effects of back-to-back hurricanes on the underwater light regime on a coral reef. Marine Biology 166 (2): 20–28.  https://doi.org/10.1007/s00227-018-3459-z.CrossRefGoogle Scholar
  35. Emanuel, Kerry. 2005. Increasing destructiveness of tropical cyclones over the past 30 years. Nature 436: 686–688.CrossRefGoogle Scholar
  36. Emanuel, Kerry A. 2013. Downscaling CMIP5 climate models shows increased tropical cyclone activity over the 21st century. Proceedings of the National Academy of Sciences 110: 12219–12224.CrossRefGoogle Scholar
  37. Ennis, Rosmin S., Marilyn E. Brandt, Kristin R. Wilson Grimes, and Tyler B. Smith. 2016. Coral reef health response to chronic and acute changes in water quality in St. Thomas, United States Virgin Islands. Marine Pollution Bulletin 111 (1-2): 418–427.CrossRefGoogle Scholar
  38. Fenner, Douglas P. 1991. Effects of Hurricane Gilbert on coral reefs, fishes and sponges at Cozumel, Mexico. Bulletin of Marine Science 48: 719–730.Google Scholar
  39. Gardner, Toby A., Isabelle M. Côté, Jennifer A. Gill, Alastair Grant, and Andrew R. Watkinson. 2005. Hurricanes and Caribbean coral reefs: Impacts, recovery patterns, and role in long-term decline. Ecology 86: 174–184.CrossRefGoogle Scholar
  40. Gochfeld, Deborah J., Carmen Schlöder, and Robert W. Thacker. 2007. Sponge community structure and disease prevalence on coral reefs in Bocas del Toro, Panama. In Porifera research: biodiversity, innovation, and sustainability, ed. Márcio R. Custódio, Gisele Lôbo-Hajdu, Eduardo Hajdu, and Guilherme Muricy, 335–343. Rio de Janeiro: Museu Nacional Série Livros 28.Google Scholar
  41. Hoegh-Guldberg, O., P.J. Mumby, A.J. Hooten, R.S. Steneck, P. Greenfield, E. Gomez, C.D. Harvell, P.F. Sale, A.J. Edwards, K. Caldeira, N. Knowlton, C.M. Eakin, R. Iglesias-Prieto, N. Muthiga, R.H. Bradbury, A. Dubi, and M.E. Hartziolos. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318 (5857): 1737–1742.CrossRefGoogle Scholar
  42. Hosseini, S.R., M. Scaini, and M. Marani. 2018. On the influence of global warming on Atlantic hurricane frequency. The International Archives of the Photogrammetry, Remote Sensing and Spatial Information Sciences 42: 527–532.CrossRefGoogle Scholar
  43. Hughes, Terrence P. 1994. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265 (5178): 1547–1551.CrossRefGoogle Scholar
  44. Hughes, T.P., and J.H. Connell. 1999. Multiple stressors on coral reefs: A long-term perspective. Limnology and Oceanography 44: 932–940.CrossRefGoogle Scholar
  45. Jackson, Jeremy B.C., Mary K. Donovan, Katie L. Cramer, and Vivian V. Lam, eds. 2014. Status and trends of Caribbean coral reefs: 1970-2012. Gland: Global Coral Reef Monitoring Network, IUCN.Google Scholar
  46. Knutson, Thomas R., John L. McBride, Johnny Chan, Kerry Emanuel, Greg Holland, Chris Landsea, Isaac Held, James P. Kossin, A.K. Srivastava, and Masato Sugi. 2010. Tropical cyclones and climate change. Nature Geoscience 3 (3): 157–163.  https://doi.org/10.1038/NGEO779.CrossRefGoogle Scholar
  47. Kuffner, I.B., L.J. Walters, M.A. Becerro, V.J. Paul, R. Ritson-Williams, and K.S. Beach. 2006. Inhibition of coral recruitment by macroalgae and cyanobacteria. Marine Ecology Progress Series 323: 107–117.CrossRefGoogle Scholar
  48. Lirman, D., and P. Fong. 1997. Patterns of damage to the branching coral Acropora palmata following Hurricane Andrew: Damage and survivorship of hurricane-generate asexual recruits. Journal of Coastal Research 13: 67–72.Google Scholar
  49. Maldonado, Manuel, and Ana Riesgo. 2008. Reproduction in the phylum Porifera: A synoptic overview. Treballs de la Societat Catalana de Biologia 59: 29–49.Google Scholar
  50. Maldonado, Manuel, and Craig M. Young. 1996. Effects of physical factors on larval behavior, settlement and recruitment of four tropical demosponges. Marine Ecology Progress Series 138: 169–180.CrossRefGoogle Scholar
  51. McMurray, Steven E., Timothy P. Henkel, and Joseph R. Pawlik. 2010. Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. Ecology 91 (2): 560–570.CrossRefGoogle Scholar
  52. Miloslavich, Patricia, Juan Manuel Díaz, Eduardo Klein, Juan José Alvarado, Cristina Díaz, Judith Gobin, Elva Escobar-Briones, Juan José Cruz-Motta, Ernesto Weil, Jorge Cortés, Ana Carolina Bastidas, Ross Robertson, Fernando Zapata, Alberto Martín, Julio Castillo, Aniuska Kazandjian, and Manuel Ortiz. 2010. Marine biodiversity in the Caribbean: Regional estimates and distribution patterns. PLoS One 5 (8): e11916.  https://doi.org/10.1371/journal.pone.0011916.CrossRefGoogle Scholar
  53. National Hurricane Center. 2018. https://www.nhc.noaa.gov/gis/. Accessed 21 Sept 2018.
  54. National Oceanic and Atmospheric Administration Office for Coastal Management. 2018. https://www.coast.noaa.gov/hurricanes/. Accessed 15 Sept 2018.
  55. National Oceanic and Atmospheric Administration National Buoy Data Center. 2018. https://www.ndbc.noaa.gov/station_history.php?station=41052. Accessed 15 Sept 2018.
  56. Nemeth, Richard S., and Joshua S. Nowlis. 2001. Monitoring the effects of land development on the near-shore reef environment of St. Thomas, USVI. Bulletin of Marine Science 69: 759–775.Google Scholar
  57. Norström, Albert V., Magnus Nyström, Jerker Lokrantz, and Carl Folke. 2009. Alternative states on coral reefs: Beyond coral–macroalgal phase shifts. Marine Ecology Progress Series 376: 295–306.CrossRefGoogle Scholar
  58. Nyström, Magnus, Carl Folke, and Fredrik Moberg. 2000. Coral reef disturbance and resilience in a human-dominated environment. Trends in Ecology & Evolution 15: 413–417.CrossRefGoogle Scholar
  59. Pasch, Richard J., Andrew B. Penny, and Robbie Berg. 2018. Hurricane Maria (AL152017). National Hurricane Center Tropical Cyclone Report. 48 pp.Google Scholar
  60. Paul, Valerie J., Ilsa B. Kuffner, Linda J. Walters, Raphael Ritson-Williams, Kevin S. Beach, and Mikel A. Becerro. 2011. Chemically mediated interactions between macroalgae Dictyota spp. and multiple life-history stages of the coral Porites astreoides. Marine Ecology Progress Series 426: 161–170.CrossRefGoogle Scholar
  61. Pawlik, Joseph R., Timothy P. Henkel, Steven E. McMurray, Susanna López-Legentil, Tse-Lynn Loh, and Sven Rohde. 2008. Patterns of sponge recruitment and growth on a shipwreck corroborate chemical defense resource trade-off. Marine Ecology Progress Series 368: 137–143.CrossRefGoogle Scholar
  62. Richards, Vincent P., Andrea M. Bernard, Kevin A. Feldheim, and Mahmood S. Shivji. 2016. Patterns of population structure and dispersal in the long-lived “redwood” of the coral reef, the giant barrel sponge (Xestospongia muta). Coral Reefs 35: 1097–1107.CrossRefGoogle Scholar
  63. Ritson-Williams, Raphael, Suzanne N. Arnold, Nicole D. Fogarty, Robert S. Steneck, Mark J.A. Vermeij, and Valerie J. Paul. 2009. New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithsonian Contributions to the Marine Sciences 38: 437–457.CrossRefGoogle Scholar
  64. Roff, George, and Peter J. Mumby. 2012. Global disparity in the resilience of coral reefs. Trends in Ecology & Evolution 27: 404–413.CrossRefGoogle Scholar
  65. Roff, George, Iliana Chollet, Christopher Doropoulos, Yimnang Golbuu, Robert S. Steneck, Adelle L. Isechal, Robert van Woesik, and Peter J. Mumby. 2015. Exposure-driven macroalgal phase shift following catastrophic disturbance on coral reefs. Coral Reefs 34: 715–725.CrossRefGoogle Scholar
  66. Rogers, Caroline S., and Jeff Miller. 2006. Permanent ‘phase shifts’ or reversible declines in coral cover? Lack of recovery of two coral reefs in St. John, US Virgin Islands. Marine Ecology Progress Series 306: 103–114.CrossRefGoogle Scholar
  67. Rogers, Caroline S., Jeff Miller, Erinn M. Muller, Peter Edmunds, Richard S. Nemeth, James P. Beets, Alan M. Friedlander, Tyler B. Smith, Rafe Boulon, Christopher F.G. Jeffrey, Charles Menza, Chris Caldow, Nasseer Idrisi, Barbara Kojis, Mark E. Monaco, Anthony Spitzack, Elizabeth H. Gladfelter, John C. Ogden, Zandy Hillis-Starr, Ian Lundgren, William Bane Schill, Ilsa B. Kuffner, Laurie L. Richardson, Barry E. Devine, and Joshua D. Voss. 2008. Ecology of coral reefs in the US Virgin Islands. In Coral reefs of the USA, ed. Bernhard M. Riegl and Richard E. Dodge, 303–373. Dordrecht: Springer.CrossRefGoogle Scholar
  68. Rose, Christopher S., and Michael J. Risk. 1985. Increase in Cliona delitrix infestation of Montastrea cavernosa heads on an organically polluted portion of the Grand Cayman fringing reef. PSZN Marine Ecology 6: 345–363.CrossRefGoogle Scholar
  69. Rützler, Klaus, Carla Piantoni, Rob W.M. Van Soest, and M. Cristina Díaz. 2014. Diversity of sponges (Porifera) from cryptic habitats on the Belize barrier reef near Carrie Bow Cay. Zootaxa 3805: 1–129.  https://doi.org/10.11646/zootaxa.3805.1.1.CrossRefGoogle Scholar
  70. Smith, T.B., R.S. Nemeth, J. Blondeau, J.M. Calnan, E. Kadison, and S. Herzlieb. 2008. Assessing coral reef health across onshore to offshore stress gradients in the US Virgin Islands. Marine Pollution Bulletin 56 (12): 1983–1991.CrossRefGoogle Scholar
  71. Smith, T.B., R.S. Ennis, E. Kadison, R.S. Nemeth, and L. Henderson. 2016a. The United States Virgin Islands Territorial Coral Reef Monitoring Program. 2016 annual report, 286 pp. Charlotte Amalie: University of the Virgin Islands.Google Scholar
  72. Smith, Tyler B., Viktor W. Brandtneris, Miguel Canals, Marilyn E. Brandt, Justin Martens, Robert S. Brewer, Elizabeth Kadison, Matthew Kammann, Jessica Keller, and Daniel M. Holstein. 2016b. Potential structuring forces on a shelf edge upper mesophotic coral ecosystem in the US Virgin Islands. Frontiers in Marine Science 3: 115.  https://doi.org/10.3389/fmars.2016.00115.CrossRefGoogle Scholar
  73. Sobel, Adam H., Suzana J. Carmago, Timothy M. Hall, Chia-Ying Lee, and Michael K. Tippett. 2016. Human influence on tropical cyclone intensity. Science 353 (6296): 242–246.CrossRefGoogle Scholar
  74. Stevely, John M., Donald E. Sweat, Theresa M. Bert, Carina Sim-Smith, and Michelle Kelly. 2011. Sponge mortality at Marathon and Long Key, Florida: Patterns of species response and population recovery. Proceedings of the 63rd Gulf and Caribbean Fisheries Institute 63: 384–400.Google Scholar
  75. Stoddart, D.R. 1969. Post-hurricane changes on the British Honduras reefs and cays: Re-survey of 1965. Atoll Research Bulletin 131: 1–36.CrossRefGoogle Scholar
  76. Van Soest, W.M. Rob, Nicole Boury-Esnault, Jean Vacelet, Martin Dohrmann, Dirk Erpenbeck, Nicole J. De Voogd, Nadiezhda Santodomingo, Bart Vanhoorne, Michelle Kelly, and John N.A. Hooper. 2012. Global diversity of sponges (Porifera). PLoS One 7 (4): e35105.  https://doi.org/10.1371/journal.pone.0035105.CrossRefGoogle Scholar
  77. Van Woesik, R., L.M. de Vantier, and J.S. Glazebrook. 1995. Effects of Cyclone ‘Joy’ on nearshore coral communities of the Great Barrier Reef. Marine Ecology Progress Series 128: 261–270.CrossRefGoogle Scholar
  78. Villamizar, Estrella, María C. Díaz, Klaus Rützler, and Renato De Nóbrega. 2013. Biodiversity, ecological structure, and change in the sponge community of different geomorphological zones of the barrier fore reef at Carrie Bow Cay, Belize. Marine Ecology 2013: 1–11.  https://doi.org/10.1111/maec.12099.CrossRefGoogle Scholar
  79. Vroom, Peter, Linda Walters, Kevin Beach, James Coyer, Jennifer Smith, Marie-Josée Abgrall, Dorothy Byron, Kathryn DeAngelis, Brenda Konar, Julie Liss, Ryan Okano, Cassandra Roberts, Laura Herren, Monica Woo, and Celia Smith. 2005. Hurricane-induced propagation and rapid regrowth of the weedy brown alga Dictyota in the Florida Keys. Florida Scientist 68: 161–174.Google Scholar
  80. Ward-Paige, Christine A., Michael J. Risk, Owen A. Sherwood, and Walter C. Jaap. 2005. Clionid sponge surveys on the Florida Reef Tract suggest land-based nutrient inputs. Marine Pollution Bulletin 51 (5-7): 570–579.CrossRefGoogle Scholar
  81. Wilkinson, C., and D. Souter. 2008. Status of Caribbean coral reefs after bleaching and hurricanes in 2005. Townsville: Global Coral Reef Monitoring Network, and Reef and Rainforest Research Centre.Google Scholar
  82. Woodley, J.E., E.A. Chornesky, P.A. Clifford, J.B.C. Jackson, L.S. Kaufman, N. Knowlton, J.C. Lang, M.P. Pearson, J.W. Porter, M.C. Rooney, K.W. Rylaarsdam, V.J. Tunnicliffe, C.M. Wahle, J.L. Wulff, A.S.G. Curtis, M.D. Dallmeyer, B.P. Jupp, M.A.R. Koehl, J. Neilgel, and E.M. Sides. 1981. Hurricane Allen’s impact on Jamaican coral reefs. Science 214 (4522): 749–755.CrossRefGoogle Scholar
  83. Wulff, J.L. 1995. Effects of a hurricane on survival and orientation of large erect coral reef sponges. Coral Reefs 14: 55–61.CrossRefGoogle Scholar
  84. Wulff, J.L. 2006. Resistance vs recovery: Morphological strategies of coral reef sponges. Functional Ecology 20: 699–708.CrossRefGoogle Scholar
  85. Wulff, Janie. 2012. Ecological interactions and the distribution, abundance, and diversity of sponges. Advances in Marine Biology 61: 273–344.CrossRefGoogle Scholar
  86. Wulff, Janie. 2013. Recovery of sponges after extreme mortality events: Morphological and taxonomic patterns in regeneration versus recruitment. Integrative and Comparative Biology 53 (3): 512–523.CrossRefGoogle Scholar
  87. Wullf, Janie L. 1991. Asexual fragmentation, genotype success, and population dynamics of erect branching sponges. Journal of Experimental Marine Biology and Ecology 149: 227–247.CrossRefGoogle Scholar
  88. Zea, Sven. 1993. Recruitment of demosponges (Porifera, Demospongiae) in rocky and coral reef habitats of Santa Marta, Colombian Caribbean. PSZNI: Marine Ecology 14: 1–21.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2020

Authors and Affiliations

  1. 1.National Center for Natural Products ResearchUniversity of MississippiUniversityUSA
  2. 2.Department of BioMolecular SciencesUniversity of MississippiUniversityUSA
  3. 3.Department of Biological SciencesUniversity of AlabamaTuscaloosaUSA
  4. 4.Harbor Branch Oceanographic Institute and Harriet L. Wilkes Honors CollegeFlorida Atlantic UniversityFort PierceUSA
  5. 5.Center for Marine and Environmental StudiesUniversity of the Virgin IslandsSt. ThomasUSA

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