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Ecological succession of the sponge cryptofauna in Hawaiian reefs add new insights to detritus production by pioneering species

  • Rapacciuolo, G. & Blois, J. L. Understanding ecological change across large spatial, temporal and taxonomic scales: Integrating data and methods in light of theory. Ecography 42, 1247–1266 (2019).

    Google Scholar 

  • Cowles, H. C. The ecological relations of the vegetation on the sand dunes of Lake Michigan. Part I. Geographical relations of the Dune Floras. Bot. Gaz. 27, 95–117 (1899).

    Article 

    Google Scholar 

  • Gleason, H. A. The individualistic concept of the plant association. Bull. Torrey Bot. Club 53, 7–26 (1926).

    Article 

    Google Scholar 

  • Denslow, J. S. Patterns of plant species diversity during succession under different disturbance regimes. Oecologia 46, 18–21 (1980).

    ADS 
    PubMed 
    Article 

    Google Scholar 

  • Budowski, G. Studies on Forest Succession in Costa Rica und Panama. Ph.D. Thesis, Yale University, New Haven (1961).

  • Opler, P. A., Baker, H. G. & Frankie, G. W. Plant reproductive characteristics during secondary succession in neotropical lowland forest ecosystems. Biotropica 12, 40–46 (1980).

    Article 

    Google Scholar 

  • Clements, F. E. Plant Succession: An Analysis of Development in Vegetation (Carnegie Institute, Washington, 1916).

    Book 

    Google Scholar 

  • Grigg, R. W. & Maragos, J. E. Recolonization of hermatypic corals on submerged lava flows in Hawaii. Ecology 55, 387–395 (1974).

    Article 

    Google Scholar 

  • Tomascik, T., Van Woesik, R. & Mah, A. J. Rapid coral colonization of a recent lava flow following a volcanic eruption, Banda Islands, Indonesia. Coral Reefs 15, 169–175 (1996).

    ADS 
    Article 

    Google Scholar 

  • McClanahan, T. R. Primary succession of coral-reef algae: Differing patterns on fished versus unfished reefs. J. Exp. Mar. Biol. Ecol. 218, 77–102 (1997).

    Article 

    Google Scholar 

  • Reaka-Kudia, M. L. The global biodiversity of coral reefs: A comparison with rain forests. In Biodiversity II: Understanding and Proteting our Biological Resources (eds Reaka-Kudla, M. et al.) 83–108 (Joseph Henry Press, 1997).

    Google Scholar 

  • Ginsburg, R. N. Geological and biological roles of cavities in coral reefs. In Perspectives on Coral Reefs (ed. Barnes, D. J.) 148–153 (Australian Institute of Marine Science, Manuka, A.C.T., Australia, 1983).

  • Fautin, D. et al. An overview of marine biodiversity in United States waters. PLoS ONE 5, e11914 (2010).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Pearman, J. K., Anlauf, H., Irigoien, X. & Carvalho, S. Please mind the gap—Visual census and cryptic biodiversity assessment at central Red Sea coral reefs. Mar. Environ. Res. 118, 20–30 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Kobluk, D. R. & Van Soest, R. W. M. Cavity-dwelling sponges in a southern Caribbean coral reef and their paleontological implications. Bull. Mar. Sci. 44, 1207–1235 (1989).

    Google Scholar 

  • Richter, C. & Wunsch, M. Cavity-dwelling suspension feeders in coral reefs – A new link in reef trophodynamics. Mar. Ecol. Prog. Ser. 188, 105–116 (1999).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • Wunsch, M., Al-Moghrabi, S. M. & Kötter, I. Communities of coral reef Cavities in Jordan, Gulf of Aqaba (Red Sea). In Proceedings of 9th International Coral Reef Symposium, Vol. 1 (2000).

  • Kornder, N. A. et al. Implications of 2D versus 3D surveys to measure the abundance and composition of benthic coral reef communities. Coral Reefs 40, 1137–1153 (2021).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Richter, C., Wunsch, M., Rasheed, M., Kötter, I. & Badran, M. I. Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature 413, 726–730 (2001).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • De Goeij, J. M. & Van Duyl, F. C. Coral cavities are sinks of dissolved organic carbon (DOC). Limnol. Oceanogr. 52, 2608–2617 (2007).

    ADS 
    Article 

    Google Scholar 

  • Slattery, M., Gochfeld, D. J., Easson, C. G. & O’Donahue, L. R. K. Facilitation of coral reef biodiversity and health by cave sponge communities. Mar. Ecol. Prog. Ser. 476, 71–86 (2013).

    ADS 
    Article 

    Google Scholar 

  • McMurray, S. E., Stubler, A. D., Erwin, P. M., Finelli, C. M. & Pawlik, J. R. A test of the sponge-loop hypothesis for emergent Caribbean reef sponges. Mar. Ecol. Prog. Ser. 588, 1–14 (2018).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • De Goeij, J. M., Van Den Berg, H., Van Oostveen, M. M., Epping, E. H. G. & Van Duyl, F. C. Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Mar. Ecol. Prog. Ser. 357, 139–151 (2008).

    ADS 
    Article 
    CAS 

    Google Scholar 

  • De Goeij, J. M. et al. Surviving in a marine desert: The sponge loop retains resources within coral reefs. Science (80-) 342, 108–110 (2013).

    ADS 
    Article 
    CAS 

    Google Scholar 

  • Rix, L. et al. Reef sponges facilitate the transfer of coral-derived organic matter to their associated fauna via the sponge loop. Mar. Ecol. Prog. Ser. 589, 85–96 (2018).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • De Goeij, J. M., Lesser, M. P. & Pawlik, J. R. Nutrient fluxes and ecological functions of coral reef sponges in a changing ocean. In Climate Change, Ocean Acidification and Sponges: Impacts Across Multiple Levels of Organization (Springer, 2017). https://doi.org/10.1007/978-3-319-59008-0_8.

  • Choi, D. R. Ecological succession of reef cavity-dwellers (coelobites) in coral rubble. Bull. Mar. Sci. 35, 72–79 (1984).

    Google Scholar 

  • Jackson, J. B. C. Competition on marine hard substrata: The adaptive significance of solitary and colonial strategies. Am. Nat. 111, 743–767 (1977).

    Article 

    Google Scholar 

  • Kobluk, D. R. Cryptic faunas in reefs: Ecology and geologic importance. Palaios 3, 379–390 (1988).

    ADS 
    Article 

    Google Scholar 

  • Hooper, J. N. A. & Van Soest, R. W. M. Class Demospongiae Sollas, 1885. In Systema Porifera (2002). https://doi.org/10.1007/978-1-4615-0747-5_3.

  • Rützler, K. The role of sponges in the mesoamerican barrier-reef ecosystem, Belize. Adv. Mar. Biol. 61, 211–271 (2012).

    PubMed 
    Article 

    Google Scholar 

  • Wulff, J. Ecological interactions and the distribution, abundance, and diversity of sponges. Adv. Mar. Biol. 61, 273–344 (2012).

    PubMed 
    Article 

    Google Scholar 

  • Riesgo, A. et al. Inferring the ancestral sexuality and reproductive condition in sponges (Porifera). Zool. Scr. 43, 101–117 (2014).

    Article 

    Google Scholar 

  • Pawlik, J. R., Chanas, B., Toonen, R. J. & Fenical, W. Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar. Ecol. Prog. Ser. 127, 183–194 (1995).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • Leong, W. & Pawlik, J. R. Evidence of a resource trade-off between growth and chemical defenses among Caribbean coral reef sponges. Mar. Ecol. Prog. Ser. 406, 71–78 (2010).

    ADS 
    Article 

    Google Scholar 

  • Maldonado, M. & Bergquist, P. R. Phylum porifera. In Atlas of Marine Invertebrates (ed. Young, C.) 21–50 (Academic, 2002).

    Google Scholar 

  • Lanna, E. & Klautau, M. Life history and reproductive dynamics of the cryptogenic calcareous sponge Sycettusa hastifera (Porifera, Calcarea) living in tropical rocky shores. J. Mar. Biol. Assoc. U. K. 98, 505–514 (2018).

    Article 

    Google Scholar 

  • Lanna, E., Monteiro, L. C. & Klautau, M. Life cycle of Paraleucilla magna Klautau, Monteiro and Borojevic, 2004 (Porifera, Calcarea). In Porifera Research: Biodiversity, Innovation and Sustainability 413–418 (2007).

  • Calazans, V. P. S. B. & Lanna, E. Influence of endogenous and exogenous factors on the reproductive output of a cryptogenic calcareous sponge. Mar. Biodivers. 49, 2837–2850 (2019).

    Article 

    Google Scholar 

  • Zimmerman, T. L. & Martin, J. W. Artificial reef matrix structures (ARMS): An inexpensive and effective method for collecting coral reef-associated invertebrates. Gulf Caribb. Res. 16, 59–64 (2004).

    Article 

    Google Scholar 

  • Brainard, R. et al. Autonomous reef monitoring structures (ARMS): A tool for monitoring indices of biodiversity in the Pacific Islands. In 11th Pacific Science Inter-Congress, Papeete, Tahiti (2009).

  • Knowlton, N. et al. Coral reef biodiversity. In Life in the World’s Oceans: Diversity, Distribution, and Abundance 65–74 (2010). https://doi.org/10.1002/9781444325508.ch4.

  • Timmers, M. A., Vicente, J., Webb, M., Jury, C. P. & Toonen, R. J. Sponging up diversity: Evaluating metabarcoding performance for a taxonomically challenging phylum within a complex cryptobenthic community. Environ. DNA https://doi.org/10.1002/edn3.163 (2020).

    Article 

    Google Scholar 

  • Vicente, J. et al. Unveiling hidden sponge biodiversity within the Hawaiian reef cryptofauna. Coral Reefs https://doi.org/10.1007/s00338-021-02109-7 (2021).

    Article 

    Google Scholar 

  • Grottoli, A. G. et al. Increasing comparability among coral bleaching experiments. Ecol. Appl. 31, e02262 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Rodgers, K. S., Jokiel, P. L., Brown, E. K., Hau, S. & Sparks, R. Over a decade of change in spatial and temporal dynamics of Hawaiian coral reef communities. Pac. Sci. 69, 1–13 (2015).

    Article 

    Google Scholar 

  • Franklin, E. C., Jokiel, P. L. & Donahue, M. J. Predictive modeling of coral distribution and abundance in the Hawaiian Islands. Mar. Ecol. Prog. Ser. 481, 121–132 (2013).

    ADS 
    Article 

    Google Scholar 

  • Jury, C. et al. Experimental reef communities persist under future ocean acidification and warming. Res. Sq. (2021).

  • Gorospe, K. D. et al. Local biomass baselines and the recovery potential for Hawaiian coral reef fish communities. Front. Mar. Sci. 5, 162 (2018).

    Article 

    Google Scholar 

  • Timmers, M. A. et al. Biodiversity of coral reef cryptobiota shuffles but does not decline under the combined stressors of ocean warming and acidification. Proc. Natl. Acad. Sci. 118(39), e2103275118 (2021).

  • Wörheide, G. & Erpenbeck, D. DNA taxonomy of sponges—Progress and perspectives. J. Mar. Biol. Assoc. U. K. 87, 1629–1633 (2007).

    Article 
    CAS 

    Google Scholar 

  • R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing (2020). https://doi.org/10.1017/CBO9781107415324.004.

  • Oksanen, J. et al. Package vegan. Community Ecology Packaging version 2, 1-295 (2013).

  • Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & Team, R. C. nlme: Linear and nonlinear mixed effects models (2020).

  • Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).

    Article 

    Google Scholar 

  • Lenth, R. V. Least-squares means: The R package. J. Stat. Softw. 69, 1–33 (2016).

    Article 

    Google Scholar 

  • Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).

    MATH 
    Book 

    Google Scholar 

  • Ribeiro, B., Padua, A., Paiva, P. C., Custódio, M. R. & Klautau, M. Exploitation of micro refuges and epibiosis: Survival strategies of a calcareous sponge. J. Mar. Biol. Assoc. U. K. 98, 495–503 (2018).

    Article 

    Google Scholar 

  • Bahr, K. D., Jokiel, P. L. & Toonen, R. J. The unnatural history of Kāne’ohe bay: Coral reef resilience in the face of centuries of anthropogenic impacts. PeerJ 3, e950 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Byrne, M. Impact of ocean warming and ocean acidification on marine invertebrate life history stages: Vulnerabilities and potential for persistence in a changing ocean. Oceanogr. Mar. Biol. Annu. Rev. 49, 1–42 (2011).

    Google Scholar 

  • Barnes, D. K. A., Ashton, G. V., Morley, S. A. & Peck, L. S. 1 °C warming increases spatial competition frequency and complexity in Antarctic marine macrofauna. Commun. Biol. 4, 1–7 (2021).

    Article 

    Google Scholar 

  • Maldonado, M., Giraud, K. & Carmona, C. Effects of sediment on the survival of asexually produced sponge recruits. Mar. Biol. 154, 631–641 (2008).

    CAS 
    Article 

    Google Scholar 

  • Eckman, J. E. Hydrodynamic processes affecting benthic recruitment. Limnol. Oceanogr. 28, 241–257 (1983).

    ADS 
    Article 

    Google Scholar 

  • Palardy, J. E. & Witman, J. D. Water flow drives biodiversity by mediating rarity in marine benthic communities. Ecol. Lett. 14, 63–68 (2011).

    PubMed 
    Article 

    Google Scholar 

  • Falter, J. L., Atkinson, M. J. & Merrifield, M. A. Mass-transfer limitation of nutrient uptake by a wave-dominated reef flat community. Limnol. Oceanogr. 49, 1820–1831 (2004).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • Sale, P. F. Coexistence of coral reef fishes—A lottery for living space. Environ. Biol. Fish. 3, 85–102 (1978).

    Article 

    Google Scholar 

  • Karlson, R. H. & Jackson, J. B. C. Competitive networks and community structure: A simulation study. Ecology 62, 670–678 (1981).

    Article 

    Google Scholar 

  • Hixon, M. A. Predation as a process structuring coral reef fish communities. In The Ecology of Fishes on Coral Reefs (1991). https://doi.org/10.1016/b978-0-08-092551-6.50022-2.

  • Hobson, E. S. Feeding patterns among tropical reef fishes. Am. Sci. 63, 382–392 (1975).

    ADS 

    Google Scholar 

  • Bailey-Brock, J. H. Fouling community development on an artificial reef in Hawaiian waters. Bull. Mar. Sci. 44, 580–591 (1989).

    Google Scholar 

  • Vicente, J., Toonen, R. J. & Bowen, B. W. Hawaiian green turtles graze on bioeroding sponges at Maunalua Bay, O‘ahu, Hawai‘i, Galaxea. J. Coral Reef Stud. 21, 3–4 (2019).

    Article 

    Google Scholar 

  • Vicente, J., Osberg, A., Marty, M. J., Rice, K. & Toonen, R. J. Influence of sponge palatability on the feeding preferences of the endemic Hawaiian tiger cowrie for indigenous and introduced sponges. Mar. Ecol. Prog. Ser. 647, 109–122 (2020).

    ADS 
    Article 

    Google Scholar 

  • Klumpp, D., McKinnon, A. & Mundy, C. Motile cryptofauna of a coral reef: Abundance, distribution and trophic potential. Mar. Ecol. Prog. Ser. 45, 95–108 (1988).

    ADS 
    Article 

    Google Scholar 

  • Carpenter, R. C. Invertebrate predators and grazers. In Life and Death of Coral Reefs (1997). https://doi.org/10.1007/978-1-4615-5995-5_9.

  • Glynn, P. W. & Enochs, I. C. Invertebrates and their roles in coral reef ecosystems. In Coral Reefs: An Ecosystem in Transition (2011). https://doi.org/10.1007/978-94-007-0114-4_18.

  • Ďuriš, Z., Horká, I., Juračka, P. J., Petrusek, A. & Sandford, F. These squatters are not innocent: The evidence of parasitism in Sponge-Inhabiting shrimps. PLoS ONE 6, e21987 (2011).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Pawlik, J. R. A sponge-eating worm from Bermuda: Branchiosyllis oculata (Polychaeta, Syllidae). Mar. Ecol. 4, 65–79 (1983).

    ADS 
    Article 

    Google Scholar 

  • Degoeij, J. M. et al. Cell kinetics of the marine sponge Halisarca caerulea reveal rapid cell turnover and shedding. J. Exp. Biol. 212, 3892–3900 (2009).

    CAS 
    Article 

    Google Scholar 

  • Alexander, B. E. et al. Cell turnover and detritus production in marine sponges from tropical and temperate benthic ecosystems. PLoS ONE 9, e109486 (2014).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Bart, M. C., Hudspith, M., Rapp, H. T., Verdonschot, P. F. M. & de Goeij, J. M. A deep-sea sponge loop? Sponges transfer dissolved and particulate organic carbon and nitrogen to associated fauna. Front. Mar. Sci. 8, 604879 (2021).

    Article 

    Google Scholar 

  • Pawlik, J. R. & McMurray, S. E. The emerging ecological and biogeochemical importance of sponges on coral reefs. Annu. Rev. Mar. Sci. 12, 315–337 (2020).

    ADS 
    Article 

    Google Scholar 

  • Brandl, S. J. et al. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science (80-). 364, 1189–1192 (2019).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • Buss, L. W. & Jackson, J. B. C. Competitive networks: Nontransitive competitive relationships in cryptic coral reef environments. Am. Nat. 113, 223–234 (1979).

    Article 

    Google Scholar 

  • Vicente, J., Ríos, J. A., Zea, S. & Toonen, R. J. Molecular and morphological congruence of three new cryptic Neopetrosia spp in the Caribbean. PeerJ 7, e6371–e6381 (2019).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 


  • Source: Ecology - nature.com

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    Fission in a colonial marine invertebrate signifies unique life history strategies rather than being a demographic trait