Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-23T07:47:21.845Z Has data issue: false hasContentIssue false
  • English
  • Français

Sexual reproduction of the potentially cultivable sponge Mycale phyllophila (Porifera, Demospongiae)

Published online by Cambridge University Press:  23 October 2015

Dan Huang ,
Huilong Ou ,
Dexiang Wang ,
Jun Chen  and
Shaoxiong Ding
Dan Huang
Affiliation:
Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361005, Fujian Province, China Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies, Xiamen University, Xiamen 361005, Fujian Province, China
Huilong Ou
Affiliation:
Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361005, Fujian Province, China Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies, Xiamen University, Xiamen 361005, Fujian Province, China
Dexiang Wang*
Affiliation:
Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361005, Fujian Province, China Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies, Xiamen University, Xiamen 361005, Fujian Province, China
Jun Chen
Affiliation:
Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361005, Fujian Province, China
Shaoxiong Ding
Affiliation:
Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361005, Fujian Province, China
*
Correspondence should be addressed to:D. Wang, Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361005, Fujian Province, China and Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies, Xiamen University, Xiamen 361005, Fujian Province, China email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Sponges of the Mycale genus are an important source of several bioactive metabolites. The raw materials for studies on this genus mainly come from the wild populations. However, the scarce biomass of sponges in the wild has become an obstacle to the better investigation of the active substances. To establish aquaculture methods based on the sexual reproduction of the demosponge Mycale phyllophila and solve the sponge shortage problems, the sexual reproductive cycle of this species was studied. Our investigation is the first to report the sexual reproduction of the Mycale species in the coastal waters of China. We collected the sponge specimens from Dongshan Bay (Fujian, China) monthly from June 2012 to January 2014. Small samples of approximately 8 cm3 in volume were cut from 15 sponges (10 tagged individuals and five random individuals) with surgical scissors for histological analysis. The results indicated that M. phyllophila is a hermaphroditic and viviparous species. The primary oocytes measured 30–50 μm in diameter, while mature oocytes reached 300–400 µm by engulfing nearby nurse cells. Spermatic cysts containing asynchronous cells were found throughout the mesohyl, especially adjacent to the oscula. Macromeres in the middle and micromeres in the periphery were observed as the cleavage progressed. The reproductive activity of M. phyllophila lasted for 5–6 months and peaked when the average water temperature was above 25°C. This suggests that water temperature is an important environmental factor influencing the sexual reproduction cycle.

Keywords

Mycale phyllophilasexual reproductionsponge aquaculturesponge shortagePoriferaDemospongiaeoogenesisspermatogenesisembryogenesisgametes density
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 5 , August 2016 , pp. 1073 - 1081
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abercrombie, M. (1946) Estimation of nuclear population from microtome sections. Anatomical Record 94, 239–247.CrossRefGoogle ScholarPubMed
Anand, T.P., Bhat, A.W., Shouche, Y.S., Roy, U., Siddharth, J. and Sarma, S.P. (2006) Antimicrobial activity of marine bacteria associated with sponges from the waters off the coast of South East India. Microbiological Research 161, 252–262.CrossRefGoogle ScholarPubMed
Ayling, A.L. (1980) Patterns of sexuality, asexual reproduction and recruitment in some subtidal marine Demospongiae. Biological Bulletin 158, 271–282.Google Scholar
Bewley, C.A., Debitus, C. and Faulkner, D.J. (1994) Microsclerodermins A and B. Antifungal cyclic peptides from the Lithistid sponge Microscleroderma sp. Journal of the American Chemical Society 116, 7631–7636.CrossRefGoogle Scholar
Carballo, J.L., Yañez, B., Zubía, E., Ortega, M.J. and Vega, C. (2010) Culture of explants from the sponge Mycale cecilia to obtain bioactive mycalazal-type metabolites. Marine Biotechnology 12, 516–525.CrossRefGoogle ScholarPubMed
Carter, G.T. and Rinehart, K.L. Jr (1978) Acarnidines, novel antiviral and antimicrobial compounds from the sponge Acarnus erithacus (de Laubenfels). Journal of the American Chemical Society 100, 4302–4304.Google Scholar
Chung, I., Huang, Y., Lee, T. and Liu, L. (2010) Reproduction of the bath sponge Spongia ceylonensis (Dictyoceratida: Spongiidae) from Penghu, Taiwan. Zoological Studies 49, 601–607.Google Scholar
Corriero, G., Liaci, L.S., Marzano, C.N. and Gaino, E. (1998) Reproductive strategies of Mycale contarenii (Porifera: Demospongiae). Marine Biology 131, 319–327.Google Scholar
Costantini, S., Romano, G., Rusolo, F., Capone, F., Guerriero, E., Colonna, G., Ianora, A., Ciliberto, G. and Costantini, M. (2015) Anti-inflammatory effects of a methanol extract from the marine sponge Geodia cydonium on the human breast cancer MCF-7 cell line. Mediators of Inflammation. doi: 10.1155/2015/204975.CrossRefGoogle ScholarPubMed
Critcher, D.J. and Pattenden, G. (1996) Synthetic studies towards pateamine, a novel thiazole-based 19-membered bis-lactone from Mycale sp. Tetrahedron Letters 37, 9107–9110.CrossRefGoogle Scholar
De Caralt, S., Otjens, H., Uriz, M.J. and Wijffels, R.H. (2007) Cultivation of sponge larvae: settlement, survival, and growth of juveniles. Marine Biotechnology 9, 592–605.CrossRefGoogle ScholarPubMed
Duckworth, A.R. and Battershill, C.N. (2003) Sponge aquaculture for the production of biologically active metabolites: the influence of farming protocols and environment. Aquaculture 221, 311–329.Google Scholar
Edrada, R.A., Heubes, M., Brauers, G., Wray, V., Berg, A., Gräfe, U., Wohlfarth, M., Mühlbacher, J. and Schaumann, K. (2002) Online analysis of Xestodecalactones AC, novel bioactive metabolites from the fungus Penicillium cf. m ontanense and their subsequent isolation from the sponge Xestospongia exigua . Journal of Natural Products 65, 1598–1604.Google Scholar
Elvin, D.W. (1976) Seasonal growth and reproduction of an intertidal sponge, Haliclona permollis (Bowerbank). Biological Bulletin 151, 108–125.CrossRefGoogle Scholar
Ereskovsky, A.V. (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. Biological Bulletin 198, 77–87.CrossRefGoogle ScholarPubMed
Ereskovsky, A.V. (2010) Development of sponges from the class Demospongiae Sollas, 1885. In Ereskovsky, A.V. (ed.) Comparative embryology of sponges. Amsterdam: Springer, pp. 47–176.CrossRefGoogle Scholar
Ereskovsky, A.V., Dubois, M., Ivanišević, J., Gazave, E., Lapebie, P., Tokina, D. and Pérez, T. (2013) Pluri-annual study of the reproduction of two Mediterranean Oscarella species (Porifera, Homoscleromorpha): cycle, sex-ratio, reproductive effort and phenology. Marine Biology 160, 423–438.CrossRefGoogle Scholar
Ettinger-Epstein, P., Whalan, S.W., Battershill, C.N. and De Nys, R. (2007) Temperature cues gametogenesis and larval release in a tropical sponge. Marine Biology 153, 171–178.Google Scholar
Fell, P.E. (1976) The reproduction of Haliclona loosanoffi and its apparent relationship to water temperature. Biological Bulletin 150, 200–210.Google Scholar
Friday, S. (2011) A study of sponge aquaculture in Jambiani: is shallow farming feasible? Independent Study Project (ISP) Collection Paper 1194.Google Scholar
Fromont, J. and Bergquist, P.R. (1994) Reproductive biology of three sponge species of the genus Xestospongia (Porifera: Demospongiae: Petrosida) from the Great Barrier Reef. Coral Reefs 13, 119–126.Google Scholar
Fusetani, N., Shinoda, K. and Matsunaga, S. (1993) Bioactive marine metabolites. 48. Cinachyrolide A: a potent cytotoxic macrolide possessing two spiro ketals from marine sponge Cinachyra sp. Journal of the American Chemical Society 115, 3977–3981.Google Scholar
Gerasimova, E.I. and Ereskovsky, A.V. (2007) Reproduction of two species of Halichondria (Demospongiae: Halichondriidae) in the White Sea. Porifera Research–Biodiversity, Innovation and Sustainability. Série Livros 28, 327–333.Google Scholar
Hajdu, E. (2015) Mycale phyllophila Hentschel, 1911. In Van Soest, R.W.M., Boury-Esnault, N., Hooper, J.N.A., Rützler, K., De Voogd, N.J., Alvarez De Glasby, B., Hajdu, E., Pisera, A.B., Manconi, R., Schoenberg, C., Janussen, D., Tabachnick, K.R., Klautau, M., Picton, B., Kelly, M., Vacelet, J., Dohrmann, M., Díaz, M.C. and Cárdenas, P. (eds) World Porifera database. http://www.marinespecies.org/porifera/porifera.php?p=taxdetails&id=713921.Google Scholar
Hawes, I., Oengpepa, C.P. and Center, W. (2010) Village scale sponge aquaculture in the Solomon Islands. Final Report for mini-project MS0506.Google Scholar
Kalinovsky, A.I., Antonov, A.S., Afiyatullov, S.S., Dmitrenok, P.S., Evtuschenko, E.V. and Stonik, V.A. (2002) Mycaloside A, a new steroid oligoglycoside with an unprecedented structure from the Caribbean sponge Mycale laxissima . Tetrahedron Letters 43, 523–525.Google Scholar
Kaye, H.R. and Reiswig, H.M. (1991) Sexual reproduction in four Caribbean commercial sponges. III. Larval behaviour, settlement and metamorphosis. Invertebrate Reproduction & Development 19, 25–35.Google Scholar
Keifer, P.A., Schwartz, R.E., Koker, M.E.S., Hughes, R.G. Jr, Rittschof, D. and Rinehart, K.L. (1991) Bioactive bromopyrrole metabolites from the Caribbean sponge Agelas conifera . Journal of Organic Chemistry 56, 2965–2975.Google Scholar
Kobayashi, J. and Ishibashi, M. (1993) Bioactive metabolites of symbiotic marine microorganisms. Chemical Reviews 93, 1753–1769.CrossRefGoogle Scholar
Krishnan, P., Balasubramaniam, M., Roy, S.D., Sarma, K., Hairun, R. and Sunder, J. (2014) Characterization of the antibacterial activity of bacteria associated with Stylissa sp., a marine sponge. Advances in Animal & Veterinary Sciences 2, 20–25.Google Scholar
Lu, P., Chueh, S., Kung, F., Pan, S., Shen, Y. and Guh, J. (2007) Ilimaquinone, a marine sponge metabolite, displays anticancer activity via GADD153-mediated pathway. European Journal of Pharmacology 556, 45–54.CrossRefGoogle ScholarPubMed
Lu, Z., Li, J., Zhang, G. and Ma, L. (2014) Ecosystem health assessment based on variable fuzzy evaluation model in Dongshan Bay, Fujian, China. Acta Ecologica Sinica 35, 4907–4919.Google Scholar
Müller, W.E.G., Wimmer, W., Schatton, W., Böhm, M., Batel, R. and Filic, Z. (1999) Initiation of an aquaculture of sponges for the sustainable production of bioactive metabolites in open systems: example, Geodia cydonium . Marine Biotechnology 1, 569–579.CrossRefGoogle ScholarPubMed
Maldonado, M. and Riesgo, A. (2009) Gametogenesis, embryogenesis, and larval features of the oviparous sponge Petrosia ficiformis (Haplosclerida, Demospongiae). Marine Biology 156, 2181–2197.Google Scholar
Mercurio, M., Corriero, G. and Gaino, E. (2007) A 3-year investigation of sexual reproduction in Geodia cydonium (Jameson 1811) (Porifera, Demospongiae) from a semi-enclosed Mediterranean bay. Marine Biology 151, 1491–1500.Google Scholar
Meroz, E. and Ilan, M. (1995) Life history characteristics of a coral reef sponge. Marine Biology 124, 443–451.Google Scholar
Miller, J.H., Singh, A.J. and Northcote, P.T. (2010) Microtubule-stabilizing drugs from marine sponges: focus on peloruside A and zampanolide. Marine Drugs 8, 1059–1079.CrossRefGoogle ScholarPubMed
Munro, M.H.G., Blunt, J.W., Dumdei, E.J., Hickford, S.J.H., Lill, R.E., Shangxiao, L., Battershill, C.N. and Duckworth, A.R. (1999) The discovery and development of marine compounds with pharmaceutical potential. Journal of Biotechnology 70, 15–25.CrossRefGoogle ScholarPubMed
Ortega, M.J., Zubía, E., Sánchez, M.C., Salvá, J. and Carballo, J.L. (2004) Structure and cytotoxicity of new metabolites from the sponge Mycale cecilia . Tetrahedron 60, 2517–2524.CrossRefGoogle Scholar
Page, M.J., Northcote, P.T., Webb, V.L., Mackey, S. and Handley, S.J. (2005) Aquaculture trials for the production of biologically active metabolites in the New Zealand sponge Mycale hentscheli (Demospongiae: Poecilosclerida). Aquaculture 250, 256–269.Google Scholar
Perry, N.B., Blunt, J.W., Munro, M.H.G. and Pannell, L.K. (1988) Mycalamide A, an antiviral compound from a New Zealand sponge of the genus Mycale . Journal of the American Chemical Society 110, 4850–4851.Google Scholar
Piel, J., Dequan, H., Gaiping, W., Butzke, D., Platzer, M., Fusetani, N. and Matsunaga, S. (2004) Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei . Proceedings of the National Academy of Sciences USA 101, 16222–16227.Google Scholar
Qu, Y., Zhang, W., Li, H., Yu, X. and Jin, M. (2005) Cultivation of marine sponges. Chinese Journal of Oceanology and Limnology 23, 194–198.Google Scholar
Reddy, A.V., Ravinder, K., Narasimhulu, M., Sridevi, A., Satyanarayana, N., Kondapi, A.K. and Venkateswarlu, Y. (2006) New anticancer bastadin alkaloids from the sponge Dendrilla cactos . Bioorganic & Medicinal Chemistry 14, 4452–4457.CrossRefGoogle ScholarPubMed
Reiswig, H.M. (1973) Coral reef project-papers in memory of Dr. Thomas F. Goreau. 8. Population dynamics of three Jamaican Demospongiae. Bulletin of Marine Science 23, 191–226.Google Scholar
Riesgo, A. and Maldonado, M. (2008) Differences in reproductive timing among sponges sharing habitat and thermal regime. Invertebrate Biology 127, 357–367.Google Scholar
Riesgo, A., Maldonado, M. and Durfort, M. (2007) Dynamics of gametogenesis, embryogenesis, and larval release in a Mediterranean homosclerophorid demosponge. Marine & Freshwater Research 58, 398–417.Google Scholar
Sakemi, S., Ichiba, T., Kohmoto, S., Saucy, G. and Higa, T. (1988) Isolation and structure elucidation of onnamide A, a new bioactive metabolite of a marine sponge, Theonella sp. Journal of the American Chemical Society 110, 4851–4853.Google Scholar
Schiefenhövel, K. and Kunzmann, A. (2012) Sponge farming trials: survival, attachment, and growth of two Indo-Pacific sponges, Neopetrosia sp. and Stylissa massa . Journal of Marine Biology. doi: 10.1155/2012/417360.Google Scholar
Shigemori, H., Bae, M.A., Yazawa, K., Sasaki, T. and Kobayashi, J. (1992) Alteramide A, a new tetracyclic alkaloid from a bacterium Alteromonas sp. associated with the marine sponge Halichondria okadai . Journal of Organic Chemistry 57, 4317–4320.Google Scholar
Simpson, J.S. and Garson, M.J. (1998) Thiocyanate biosynthesis in the tropical marine sponge Axinyssa n. sp. Tetrahedron Letters 39, 5819–5822.Google Scholar
Simpson, T.L. and Gilbert, J.J. (1974) Gemmulation, gemmule hatching, and sexual reproduction in fresh-water sponges II. Life cycle events in young, larva-produced sponges of Spongilla lacustris and an unidentified species. Transactions of the American Microscopical Society 93, 39–45.Google Scholar
Singh, A.J., Chunxiao, X., Xiaoming, X., West, L.M., Wilmes, A., Chan, A., Hamel, E., Miller, J.H., Northcote, P.T. and Ghosh, A.K. (2009) Peloruside B, a potent antitumor macrolide from the New Zealand marine sponge Mycale hentscheli: isolation, structure, total synthesis, and bioactivity. Journal of Organic Chemistry 75, 2–10.Google Scholar
Southwood, T.R.E., May, R.M., Hassell, M.P. and Conway, G.R. (1974) Ecological strategies and population parameters. American Naturalist 108, 791–804.Google Scholar
Wahab, M.A.A., De Nys, R. and Whalan, S.W. (2012) Closing the life cycle for the sustainable aquaculture of the bath sponge Coscinoderma matthewsi . Aquaculture 324, 281–289.Google Scholar
Wellington, K.D., Cambie, R.C., Rutledge, P.S. and Bergquist, P.R. (2000) Chemistry of Sponges. 19. Novel bioactive metabolites from Hamigera tarangaensis . Journal of Natural Products 63, 79–85.Google Scholar
West, L.M., Northcote, P.T., Hood, K.A., Miller, J.H. and Page, M.J. (2000) Mycalamide D, a new cytotoxic amide from the New Zealand marine sponge Mycale species. Journal of Natural Products 63, 707–709.Google Scholar
Whalan, S.W., Battershill, C.N. and De Nys, R. (2007) Sexual reproduction of the brooding sponge Rhopaloeides odorabile . Coral Reefs 26, 655–663.Google Scholar
Zheng, L., Chen, H., Han, X., Lin, W. and Yan, X. (2005) Antimicrobial screening and active compound isolation from marine bacterium NJ6-3-1 associated with the sponge Hymeniacidon perleve . World Journal of Microbiology and Biotechnology 21, 201–206.Google Scholar