Abstract
This study presents the phenology of two common Mediterranean sponges belonging to the genus Oscarella (Porifera, Homoscleromorpha). Oscarella tuberculata and Oscarella lobularis are two sibling species, dwellers of shallow benthic communities which tend to have distinct ecological behavior, respectively, euryecious and rather stenoecious. The comparative study of their reproductive cycle showed that both Oscarella species have a seasonal reproductive cycle with a successive phase duration differing from one species to another. In both species, there is a continuous oogenesis, with new oocytes appearing in spring, whereas the spermatogenesis generally starts later with the early warming of the sea. The embryonic development and the larval release are restricted to the warmest months of the year. We also observed a shift in the period of gametogenesis and larval emission depending on species and differences in their sensitivity to changes in thermal regime. It appears that an increase in seawater temperature can affect sex determination, with mainly a shift toward males in both species. Their reproductive efforts are variable in time, and can be in some cases influenced by the temperature regime. This is especially the case of O. lobularis which seems to be the most thermosensitive, its phenology responding significantly to changes in thermal regime, whereas O. tuberculata seems to be less sensitive and/or reactive. By detecting phenological changes among sponges, this study demonstrated the relevance of such monitoring to assess the possible biological response to climate change.
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References
Adiyodi KG, Adiyodi RG (eds) (1993) Reproductive biology of invertebrates. 6 A: a sexual propagation and reproductive strategies. Oxford & IBH publishing Co, New Delhi
Baccetti B, Gaino E, Sarà M (1986) A sponge with acrosome: Oscarella lobularis. J Ultrastr Mol Struct Res 94:195–198
Baldacconi R, Nonnis-Marzano C, Gaino E, Corriero G (2007) Sexual reproduction, larval development and release in Spongia offcinalis L. (Porifera, Demospongiae) from the Apulian coast. Mar Biol 152:969–979
Bates WR (2005) Environmental factors affecting reproduction and development in ascidians and other protochordates. Canad J Zool 83:51–61
Beiring EA, Lasker HR (2000) Egg production by colonies of a gorgonian coral. Mar Ecol Progr Ser 196:169–177
Boury-Esnault N, Jamieson BGM (1999) Porifera. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrayes. 9: Pt a Progress in male gamete biology. Oxford & IBH Publishing Co. PVT. LTD, New Delhi, pp 1–41
Boury-Esnault N, Solé-Cava AM, Thorpe JP (1992) Genetic and cytological divergence betwen colour morphs of the Mediterranean sponge Oscarella lobularis Schmidt (Porifera, Demospongiae, Oscarellidae). J Nat Hist 26:271–284
Boury-Esnault N, Ereskovsky AV, Bézac C, Tokina D (2003) Larval development in Homoscleromorpha (Porifera, Demospongiae) first evidence of basal membrane in sponge larvae. Invertebr Biol 122:187–202
Cerrano C, Arillo A, Azzini F, Calcinai B, Castellano L, Muti C, Valisano L, Zega G, Bavestrello G (2005) Gorgonian population recovery after a mass mortality event. Aquat Conservat: Mar Freshw Ecosyst 15:147–157
Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton
Corriero G, Sara M, Vaccaro P (1996) Sexual and asexual reproduction in two species of Tethya (Porifera, Demospongiae) from a Mediterranean coastal lagoon. Mar Biol 126:175–181
Corriero G, Scalera Liaci L, Marzano N, Gaino E (1998) Reproductive strategies of Mycale contarenii (Porifera: Demospongia). Mar Biol 131:319–328
de Caralt S, Uriz MJ, Ereskovsky AV, Wijffels RH (2007) Embryo development of Corticium candelabrum (Demospongiae: Homosclerophorida). Invertebr Biol 126:211–219
Di Camillo CJ, Coppari M, Bartolucci I, Bo M, Betti F, Bertolino M, Calcinai M, Cerrano C, De Grandis G, Bavestrello G (2012) Temporal variations in growth and reproduction of Tedania anhelans and Chondrosia reniformis in the North Adriatic Sea. Hydrobiologia 687:299–313
Diaz JP (1973) Cycle sexuel de deux demosponges de l’étang de Thau: Suberites massa Nardo et Hymeniacidon caruncula Bowerbank. Bull Soc Zool France 98:145–156
Diaz JP (1979) Variations, différentiations et fonctions des catégories cellulaires de la demosponge d’eaux saumâtres, Suberites massa, Nardo, au cours du cycle biologique annuel et dans des conditions expérimentales. Dissertation, Montpellier
Edmunds PJ, Gates RD, Gleason DF (2001) The biology of larvae from the reef coral Porites astreoides, and their response to temperature disturbances. Mar Biol 139:981–989
Elvin DV (1976) Seasonal growth and reproduction of an intertidal sponge Haliclona permolis (Bow.). Biol Bull 151:108–125
Ereskovsky AV (2000) Reproduction cycles and strategies of cold-water sponges Halisarca dujardini (Demospongiae, Dendroceratida), Myxilla incrustans and Iophon piceus (Demospongiae, Poecilosclerida) from the White Sea. Biol Bull 198:77–87
Ereskovsky AV (2010) The comparative embryology of sponges. Springer Verlag, Dordrecht
Ereskovsky AV, Boury-Esnault N (2002) Cleavage pattern in Oscarella species (Porifera, Demospongiae, Homoscleromorpha), transmission of maternal cells and symbiotic bacteria. J Nat Hist 36:1761–1775
Ereskovsky AV, Ivanišević J, Pérez T (2009a) Overview on the Homoscleromorpha sponges diversity in the Mediterranean. In: Pergent-Martini C, Brichet M (eds) Proc First Mediterranean Symposium on the Coralligenous and other calcareous bio-concretions of the Mediterranean Sea. RAC/SPA, Tabarka, pp 88–94
Ereskovsky AV, Borchiellini C, Gazave E, Ivanišević J, Lapébie P, Pérez T, Renard-Deniel E, Vacelet J (2009b) The homoscleromorph sponge Oscarella lobularis as model in evolutionary and developmental biology. BioEssays 31:89–97
Ettinger-Epstein P, Whalan SW, Battershill CN, de Nys R (2007) Temperature cues gametogenesis and larval release in a tropical sponge. Mar Biol 153:171–178
Fell PE (1976) The reproduction of Haliclona loosanoffi and its apparent relationschip to water temperature. Biol Bull 150:200–210
Fell PE (1993) Porifera. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates Asexual Propagation and reproductive strategies, vol 6. Wiley, Chichester, pp 1–44
Fell PE, Jacob WF (1979) Reproduction and development of Halichondria sp. in the mystic estuary connecticut. Biol Bull 155:62–75
Gaino E, Burlando B, Buffa P (1986a) The vacuolar cells of Oscarella lobularis (Porifera, Demospongiae): ultrastructural organisation, origin and function. J Morphol 188:29–37
Gaino E, Burlando B, Buffa P (1986b) Contribution to the study of egg development and derivation in Oscarella lobularis (Porifera, Demospongiae). Int J Invertbr Reprod Dev 91:297–305
Gazave E, Lapébie P, Ereskovsky AV, Vacelet J, Renard E, Borchiellini C (2010) Molecular phylogeny restores the supra-generic subdivision of Homoscleromorphe (Dendy, 1905) sponges. PLoS ONE 5(12):e14290. doi:10.1371/journal.pone.0014290
Gazave E, Lapébie P, Ereskovsky AV, Vacelet J, Renard E, Cárdenas P, Borchiellini C (2012) No longer Demospongiae: homoscleromorph sponges revisited by molecular phylogeny, Linnaean classification and the PhyloCode. Hydrobiologia 687:3–10
Gerasimova EI, Ereskovsky AV (2007) Reproduction of two species of Halichondria (Demospongiae: Halichondriidae) in the White Sea. In: Custódio MR, Lôbo-Hajdu G, Hajdu E, Muricy G (eds) Porifera Research–Biodiversity, innovation and sustainability. Série Livros 28. Museu Nacional, Rio de Janeiro, pp 327–333
Ivanišević J, Thomas OP, Lejeusne C, Chevaldonne P, Pérez T (2011) Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics 7:289–304
Kaye HR, Reiswig HM (1991) Sexual reproduction in four Carribean commercial sponges. I. Reproductive cycles and spermatogenesis. Invertbr Reprod Dev 19:1–11
Lawrence AJ, Soame JM (2004) The effects of climate change on the reproduction of coastal invertebrates. Ibis 146:29–39
Lejeusne C, Chevaldonne P, Pergent-Martini C, Boudouresque CF, Pérez T (2010) Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol Evol 25:250–260
Lepore E, Sciscioli M, Liaci LS, Santarelli G, Gaino E (2000) Sexual reproduction of Cinachyra tarentina (Porifera, Demospongiae). Ital J Zool 67:153–158
Maldonado M, Riesgo A (2008) Reproductive output in a Mediterranean population of the homosclerophorid Corticium candelabrum (Porifera, Demospongiae), with notes on the ultrastructure and behavior of the larva. Mar Ecol 29:298–316
Meewis H (1938) Contribution à l’étude de l’embryogénèse des Myxospongiae: Halisarca lobularis (Schmidt). Arch Biol Liége 59:1–66
Mercurio M, Corriero G, Gaino E (2007) A 3-year investigation of sexual reproduction in Geodia cydonium (Jameson 1811) (Porifera, Demospongiae) from a semi-enclosed Mediterranean bay. Mar Biol 151:1491–1500
Meroz-Fine E, Shefer S, Ilan M (2005) Changes in morphology and physiology of an East Mediterranean sponge in different habitats. Mar Biol 147:243–250
Morrissey J, Sumich JL (2009) Introduction to the biology of marine life, 9th edn. Jones & Bartlett Publishers, Boston
Newlon AW, Yund PO, Stewart-Savage J (2003) Phenotypic plasticity of reproductive effort in a colonial ascidian, Botryllus schlosseri. J Exp Zool 297:180–188
Olive PJW (1995) Annual breeding cycles in marine invertebrates and environmental temperature: probing the proximate and ultimate causes of reproductive synchrony. J Therm Biol 20:79–90
Pérez T, Ivanisevic J, Dubois M, Pedel L, Thomas OP, Tokina D, Ereskovsky AV (2011) Oscarella balibaloi, a new sponge species (Homoscleromorpha: Plakinidae) from the Western Mediterranean Sea: cytological description, reproductive cycle and ecology. Mar Ecol 32:174–187
Pérez-Porro AR, Gonzàlez J, Uriz MJ (2012) Reproductive traits explain contrasting ecological features in sponges: the sympatric poecilosclerids Hemimycale columella and Crella elegans as examples. Hydrobiologia 687:315–330
Ribes M, Coma R, Rossi S, Micheli M (2007) Cycle of gonadal development in Eunicella singularis (Cnidaria: Octocorallia): trends in sexual reproduction in gorgonians. Invert Biol 126:307–317
Riesgo A, Maldonado M (2008) Differences in reproductive timing among sponges sharing habitat and thermal regime. Invertbr Biol 127:357–367
Riesgo A, Maldonado M, Durfort M (2007) Dynamics of gametogenesis, embryogenesis, and larval release in a Mediterranean homosclerophorid demosponge. Mar Fresh Res 58:398–417
Sarà M (1993) Porifera. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, sexual differentiation and behaviour, vol 5. Wiley, Chichester, pp 1–29
Scalera Liaci L, Sciscioli M, Matarrese A (1973) Sexual reproduction in some sponges: Chondrilla nucula O.S. and Chondrosia reniformis Nardo (Tetractinomorpha). Rap Commis Internat Explor Sci Mer Méditerranée 22:129–130
Schulze FE (1877) Untersuchungen über den bau und Entwicklung der Spongien Die Gattung Halisarca. Z Wiss Zool 28:1–48
Schulze FE (1880) Untersuchungen über den bau und Entwicklung der Spongien. Die Plakiniden. Z Wiss Zool 34:407–451
Schulze FE (1881) Untersuchungen über den bau und Entwicklung der Spongien. Zehnte Mittheilung Corticium candelabrum O. Schmidt. Z Wiss Zool 35:410–430
Simpson TL (1968) The biology of the marine sponge Microciona prolifera (Ellis and Sollander). II. Temperature-related annual chamges in functional and reproductive elements with a discription of larval metamorphosis. J Exp Mar Biol Ecol 2:252–277
Simpson TL (1984) The cell biology of Sponges. Springer, New York
Siribelli L (1962) Differenze nel ciclo sessuale di populazioni conveventi di Axinella damicornis (Esper) ed Axinella verrucosa O.S. (Demospongiae). Ann Ist Mus Zool Univ Napoli 14:1–8
Storr JF (1964) Ecology of the Gulf of Mexico commercial sponges and its relation to the fishery. Spec Sci Rep Fish 466:1–73
Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–54
Tanaka-Ichihara K, Watanabe Y (1990) Gametogenic cycle in Halichondria okadaii. In: Rützler K (ed) New perspectives in sponge biology. Press Washington, Smithsonian Inst, pp 170–174
Tuzet O, Paris J (1964) La spermatogenése, l’ovogenése, la fécondation et les premiers stades du developpement chez Octavella galangaui. Vie Milieu 15:309–327
Vishnyakov AE, Ereskovsky AV (2009) Bacterial symbionts as an additional cytological marker for identification of sponges without a skeleton. Mar Biol 156:1625–1632
Wapstra M, van Soest RWM (1987) Sexual reproduction, larval morphology and bechaviour in Demosponges from the southwest of the Netherlands. In: Boury-Esnault N, Vacelet J (eds) Taxonomy of Porifera NATO ASI Ser, vol 13. Springer, Berlin, pp 281–307
Wells HW, Wells MJ, Gray IE (1964) Ecology of sponges in Hatteras harbor, North Carolina. Ecology 45:752–767
Whalan S, Battershill C, de Nys R (2007) Variability in reproductive output across a water quality gradient for a tropical marine sponge. Mar Biol 153:163–169
Whalan S, Ettinger-Epstein P, de Nys R (2008) The effect of temperature on larval pre-settlement duration and metamorphosis for the sponge, Rhopaloeides odorabile. Coral Reefs 27:783–786
Witte U (1996) Seasonal reproduction in deep-sea sponges–triggered by vertical particle flux? Mar Biol 124:571–581
Witte U, Barthel D, Tendal O (1994) The reproductive cycle of the sponge Halichondria panicea Pallas (1766) and its relationship to temperature and salinity. J Exp Mar Biol Ecol 183:41–52
Acknowledgments
The authors are grateful to Roland Graille, Dr. Pierre Chevaldonné and Frederic Zuberer for diving assistance; to Dr. Jean-Claude Romano, Dr. Nathaniel Bensoussan and the program MEDCHANGE for the temperature data, and to Chantal Bezac for technical support. This work was partly supported by the European Marie Curie Mobility program (fellowship of T. Pérez, MEIF-CT-2003-501339, and fellowship of A. Ereskovsky, MIF1-CT-2006-040065-980066) and the ECIMAR program of the French National Agency for Research (ANR-06-BDIV-001).
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Ereskovsky, A.V., Dubois, M., Ivanišević, J. et al. 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 (2013). https://doi.org/10.1007/s00227-012-2100-9
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DOI: https://doi.org/10.1007/s00227-012-2100-9