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Phenology of sexual reproduction in the common coral reef sponge, Carteriospongia foliascens

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Abstract

Understanding processes that contribute to population maintenance is critical to the management and conservation of species. Despite this, very little is currently known about the reproductive biology of Great Barrier Reef (GBR) sponge species. Here, we established reproductive parameters including mode of sexuality and development, seasonality, sex ratios, gametogenesis, reproductive output, and size at sexual maturity for the common phototrophic intertidal sponge, Carteriospongia foliascens, in the central GBR over two reproductive cycles. A population sexual productivity index (PoSPi) integrating key reproductive parameters was formulated to compare population larval supply over time. This study shows that C. foliascens is reproductive all year round, gonochoric and viviparous, with larvae developing asynchronously throughout the mesohyl. The influence of environmental parameters relevant to C. foliascens reproduction [i.e., sea surface temperature (SST), photoperiod, and rainfall] was also examined, and SST was found to have the most significant effect on phenology. C. foliascens reproduction exhibited annual mono-cyclic patterns closely resembling SST fluctuations. Reproductive output was depressed at low SST (<23 °C) and increased at temperatures above 23 °C. Peak sperm release occurred at temperatures above 25 °C, while peak larval release occurred during the annual temperature maxima (>28 °C). A twofold increase in maximum larval production (PoSPi) in C. foliascens was observed in the second reproductive cycle, following a depressed PoSPi in the first cycle. This reduction in PoSPi in the first reproductive cycle was associated with elevated SST and rainfall, coinciding with one of the strongest La Niña events on record.

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References

  • Abdo DA, Fromont J, McDonald JI (2008) Strategies, patterns and environmental cues for reproduction in two temperate haliclonid sponges. Aquat Biol 1:291–302

    Article  Google Scholar 

  • Abdul Wahab MA, de Nys R, Whalan S (2011) Larval behaviour and settlement cues of a brooding coral reef sponge. Coral Reefs 30:451–460

    Article  Google Scholar 

  • Abdul Wahab MA, de Nys R, Whalan S (2012) Closing the lifecycle for the sustainable aquaculture of the bath sponge Coscinoderma matthewsi. Aquaculture 324–325:281–289

    Article  Google Scholar 

  • Anderson M (2005) PERMANOVA. Permutational multivariate analysis of variance, a computer program. Department of Statistics, University of Auckland:24

  • Bancroft JD, Gamble M (2008) Theory and practice of histological techniques. 6th edition. Elsevier Health Sciences. 725pp.

  • Bannister R, Battershill C, de Nys R (2012) Suspended sediment grain size and mineralogy across the continental shelf of the Great Barrier Reef: Impacts on the physiology of a coral reef sponge. Cont Shelf Res 32:86–95

    Article  Google Scholar 

  • Bautista-Guerrero E, Carballo JL, Maldonado M (2010) Reproductive cycle of the coral-excavating sponge Thoosa mismalolli (Clionaidae) from Mexican Pacific coral reefs. Invertebr Biol 129:285–296

    Article  Google Scholar 

  • Bell JJ (2008) The functional roles of marine sponges. Estuar Coast Shelf Sci 79:341–353

    Article  Google Scholar 

  • Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS (2013) Could some coral reefs become sponge reefs as our climate changes? Glob Change Biol 19:2613–2624

    Google Scholar 

  • Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, DeVantier L (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563

    Article  CAS  PubMed  Google Scholar 

  • Cohen D (1966) Optimizing reproduction in a randomly varying environment. J Theor Biol 12:119–129

    Article  CAS  PubMed  Google Scholar 

  • Colegrave N (2002) Sex releases the speed limit on evolution. Nature 420:664–666

    Article  CAS  PubMed  Google Scholar 

  • Cooper TF, Uthicke S, Humphrey C, Fabricius KE (2007) Gradients in water column nutrients, sediment parameters, irradiance and coral reef development in the Whitsunday Region, central Great Barrier Reef. Estuar Coast Shelf Sci 74:458–470

    Article  Google Scholar 

  • Corredor JE, Wilkinson CR, Vicente VP, Morell JM, Otero E (1988) Nitrate release by Caribbean reef sponges. Limnol Oceanogr 33:114–120

    Article  CAS  Google Scholar 

  • Corriero G, Liaci LS, Marzano CN, Gaino E (1998) Reproductive strategies of Mycale contarenii. Mar Biol 131:319–327

    Article  Google Scholar 

  • Crean AJ, Marshall DJ (2009) Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philos Trans R Soc Lond B Biol Sci 364:1087–1096

    Article  PubMed Central  PubMed  Google Scholar 

  • deBruyn AM, Meeuwig JJ (2001) Detecting lunar cycles in marine ecology: periodic regression versus categorical ANOVA. Mar Ecol Prog Ser 214:307–310

    Article  Google Scholar 

  • de Goeij JM, van Oevelen D, Vermeij MJA, Osinga R, Middelburg JJ, de Goeij AFPM, Admiraal (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342:108–110

    Google Scholar 

  • Diaz MC, Rützler K (2001) Sponges: An essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546

    Google Scholar 

  • Ereskovsky AV (2000) Reproduction cycles and strategies of the cold-water sponges Halisarca dujardini (Demospongiae, Halisarcida), Myxilla incrustans and Iophon piceus (Demospongiae, Poecilosclerida) from the White Sea. Biol Bull 198:77–87

    Article  CAS  PubMed  Google Scholar 

  • Ereskovsky AV, Dubois M, Ivanišević J, Gazave e, Lapebie P, Tokina D, Pérez T (2013) Pluri-annual study of the reproduction of two Mediterranean Oscarella species (Porifera, Homoscleromorpha): cycle, sex ratio, reproductive effort and phenology. Mar Biol 160:423–438

    Article  Google Scholar 

  • Ettinger-Epstein P, Whalan S, Battershill CN, de Nys R (2007) Temperature cues gametogenesis and larval release in a tropical sponge. Mar Biol 153:171–178

    Article  Google Scholar 

  • Ettinger-Epstein P, Whalan S, Battershill CN, de Nys R (2008) A hierarchy of settlement cues influences larval behaviour in a coral reef sponge. Mar Ecol Prog Ser 365:103–113

    Article  Google Scholar 

  • Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146

    Article  CAS  PubMed  Google Scholar 

  • Frøhlich H, Barthel D (1997) Silica uptake of the marine sponge Halichondria panicea in Kiel Bight. Mar Biol 128:115–125

    Article  Google Scholar 

  • Fromont J (1999) Reproduction of some demosponges in a temperate Australian shallow water habitat. Mem Qld Mus 44:485–192

    Google Scholar 

  • Fromont J, Bergquist PR (1994) Reproductive biology of three sponge species of the genus Xestospongia (Porifera: Demospongia: Petrosida) from the Great Barrier Reef. Coral Reefs 13:119–126

    Article  Google Scholar 

  • Giles BD (2012) The Australian Summer 2010/2011. Weather 67:9–12

    Article  Google Scholar 

  • Harshman LG, Zera AJ (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22:80–86

    Article  PubMed  Google Scholar 

  • Hoegh-Guldberg O, Mumby P, Hooten A, Steneck R, Greenfield P, Gomez E, Harvell C, Sale P, Edwards A, Caldeira K (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, Rapp HT, Schläppy M, Schleper C, Kuypers MMM (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11:2228–2243

    Article  CAS  PubMed  Google Scholar 

  • Hopper KR (1999) Risk-spreading and bet-hedging in insect population biology. Annu Rev Entomol 44:535–560

    Article  CAS  PubMed  Google Scholar 

  • Hughes T, Baird A, Dinsdale E, Moltschaniwskyj N, Pratchett M, Tanner J, Willis B (2000) Supply-side ecology works both ways: the link between benthic adults, fecundity, and larval recruits. Ecology 81:2241–2249

    Article  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson J, Kleypas J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  PubMed  Google Scholar 

  • Imielska A (2011) Seasonal climate summary southern hemisphere (summer 2010-2011): Second-wettest Australian summer on record and one of the strongest La Niña events on record. Aust Meteorol Oceanogr J 61:241

    Google Scholar 

  • Leong W, Pawlik JR (2011) Comparison of reproductive patterns among 7 Caribbean sponge species does not reveal a resource trade-off with chemical defenses. J Exp Mar Biol Ecol 401:80–84

    Article  Google Scholar 

  • Longo C, Pontassuglia C, Corriero G, Gaino E (2012) Life-cycle traits of Paraleucilla magna, a calcareous sponge invasive in a coastal Mediterranean basin. PloS one 7(8):e42392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maldonado M, Riesgo A (2008) Reproduction in Porifera: a synoptic overview. Treballs de la Societat Catalana de Biologia 59:29–49

  • Maldonado M, Carmona C, Velásquez Z, Puig A, Cruzado A, López A, Young CM (2005) Siliceous sponges as a silicon sink: An overlooked aspect of benthopelagic coupling in the marine cycle. Limnol Oceanogr 50:799–809

    Article  CAS  Google Scholar 

  • Mercurio M, Giuseppe C, Miriam G, Rosella B, Gaino E (2013) Sexual reproduction in Sarcotragus spinosulus from two different shallow environments. Mar Ecol 34:394–408

    Google Scholar 

  • Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233

    Article  Google Scholar 

  • Otto SP (2003) The advantages of segregation and the evolution of sex. Genetics 164:1099–1118

    PubMed Central  PubMed  Google Scholar 

  • Przeslawski R, Ahyong S, Byrne M, Wörheide G, Hutchings P (2008) Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs. Glob Change Biol 14:2773–2795

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge 537

    Book  Google Scholar 

  • Reiswig HM (1981) Partial carbon and energy budgets of the bacteriosponge Verongia fistularis (Porifera: Demospongiae). Mar Ecol 2:273–293

    Article  CAS  Google Scholar 

  • Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals: Comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Mar Ecol Prog Ser 60:185–203

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Scott A, Harrison PL. Brooks LO (2013) Reduced salinity decreases the fertilization success and larval survival of two scleractinian coral species. Mar Environ Res 92:10–14

    Google Scholar 

  • Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt K, Tignor M, Miller H (2007) Intergovernmental Panel on Climate Change, Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

  • Uriz MJ, Turon X, Becerro MA, Galera J, Lozano J (1995) Patterns of resource allocation to somatic, defensive, and reproductive functions in the Mediterranean encrusting sponge Crambe crambe (Demospongiae, Poecilosclerida). Mar Ecol Prog Ser 124:159–170

    Article  Google Scholar 

  • Usher KM, Sutton DC, Toze S, Kuo J, Fromont J (2004) Sexual reproduction in Chondrilla australiensis (Porifera : demospongiae). Mar Freshw Res 55:123–134

    Article  Google Scholar 

  • Webster NS, Luter HM, Soo RM, Botté ES, Simister RL, Abdo D, Whalan S (2012) Same, same but different: symbiotic bacterial associations in GBR sponges. Front Microbiol 3:444

    Google Scholar 

  • Whalan S, Battershill CN, de Nys R (2007a) Variability in reproductive output across a water quality gradient for a tropical marine sponge. Mar Biol 153:163–169

    Article  Google Scholar 

  • Whalan S, Battershill CN, de Nys R (2007b) Sexual reproduction of the brooding sponge Rhopaloeides odorabile. Coral Reefs 26:655–663

    Article  Google Scholar 

  • Whalan S, Ettinger-Epstein P, Battershill CN, de Nys R (2008) Larval vertical migration and hierarchical selectivity of settlement in a brooding marine sponge. Mar Ecol Prog Ser 368:145–154

    Article  Google Scholar 

  • Wilkinson CR (1983) Net primary productivity in coral reef sponges. Science 219:410–412

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson CR (1987) Productivity and abundance of large sponge populations on Flinders Reef flats, Coral Sea. Coral Reefs 5:183–188

    Article  Google Scholar 

  • Wilkinson CR (1988) Foliose Dictyoceratida of the Australian Great Barrier Reef. II Ecology and distribution of these prevalent sponges. Mar Ecol 9:321–327

    Article  Google Scholar 

  • Witte U, Barthel D (1994) Reproductive cycle and oogenesis of Halichondria panicea (Pallas) in Kiel Bight. Sponges in time and space. Balkema, Rotterdam 389–393

  • Wolanski E, Fabricius KE, Cooper TF, Humphrey C (2008) Wet season fine sediment dynamics on the inner shelf of the Great Barrier Reef. Estuar Coast Shelf Sci 77:755–762

    Article  Google Scholar 

  • Yahel G, Sharp JH, Marie D, Häse C, Genin A (2003) In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: Bulk DOC is the major source for carbon. Limnol Oceanogr 48:141–149

    Article  Google Scholar 

  • Zarrouk S, Ereskovsky AV, Mustapha KB, Abed AE, Pérez T (2013) Sexual reproduction of Hippospongia communis (Lamrk, 1814) (Dictyoceratida, Demospongiae): comparison of two populations living under contrasting environmental conditions. Mar Ecol 34:432–442

    Google Scholar 

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Acknowledgments

We would like to thank M. Vermeij and three anonymous reviewers whose advice and comments improved the final version of this manuscript. We would also like to thank our field assistants for supporting collection of sponge samples over the period of this study. M.A. Abdul Wahab is supported by a JCUPRS and AIMS@JCU scholarships. NSW was funded through an Australian Research Council Future Fellowship (FT120100480). This study was partly funded through an Australian Research Council linkage Grant with Reef HQ (LP0990664).

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Correspondence to M. A. Abdul Wahab.

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Communicated by Biology Editor Dr. Mark Vermeij

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Abdul Wahab, M.A., de Nys, R., Webster, N. et al. Phenology of sexual reproduction in the common coral reef sponge, Carteriospongia foliascens . Coral Reefs 33, 381–394 (2014). https://doi.org/10.1007/s00338-013-1119-9

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