Skip to main content
SpringerLink
Log in

Sexual reproduction of the solitary sunset cup coral Leptopsammia pruvoti (Scleractinia: Dendrophylliidae) in the Mediterranean. 1. Morphological aspects of gametogenesis and ontogenesis

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Information on the reproduction in scleractinian solitary corals and in those living in temperate zones is notably scant. Leptopsammia pruvoti is a solitary coral living in the Mediterranean Sea and along Atlantic coasts from Portugal to southern England. This coral lives in shaded habitats, from the surface to 70 m in depth, reaching population densities of >17,000 individuals m−2. In this paper, we discuss the morphological aspects of sexual reproduction in this species. In a separate paper, we report the quantitative data on the annual reproductive cycle and make an interspecific comparison of reproductive traits among Dendrophylliidae aimed at defining different reproductive strategies. The present study on L. pruvoti is the first in-depth investigation of the reproductive biology of a species of this genus. As expected for a member of the family Dendrophylliidae, L. pruvoti is a gonochoric and brooding coral. The gastrodermal tissue of the gametogenetic mesenteries we examined was swollen and granular, which led us to hypothesize that interstitial cells could have a trophic function favoring gametogenesis. Undifferentiated germ cells arose in the gastrodermis and subsequently migrated to the mesoglea, where they completed gametogenesis. During spermary development, spermary diameter increased from a minimum of 14 μm during the immature stages to a maximum of 410 μm during the mature stages. As oogenesis progressed, we observed a gradual reduction in the nucleus to cytoplasm ratio due to the steady synthesis of yolk. During the final stages of oogenesis, after having migrated to the extreme periphery of the oocyte and having firmly adhered to the oolemma, the nucleus became indented, assuming a sickle or dome shape. We can hypothesize that the nucleus’ migration and change of shape may have to do with facilitating fertilization and determining the future embryonic axis. During oogenesis, oocyte diameter increased from a minimum of 20 μm during the immature stage to a maximum of 680 μm when mature. Embryogenesis took place in the coelenteron. We did not see any evidence that even hinted at the formation of a blastocoel; embryonic development proceeded via stereoblastulae with superficial cleavage. Gastrulation took place by delamination. Early and late embryos had diameters of 204–724 μm and 290–736 μm, respectively. When released, the larvae had completed ontogenesis and swam by a ciliary movement with the aboral pole at the anterior, their shape varied from spherical to cylindrical (in the latter the oral–aboral axis measured 695–1,595 μm and the transversal one measured 267–633 μm).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2A–H
Fig. 3A–F
Fig. 4A–G
Fig. 5A–C

Similar content being viewed by others

References

  • Abe N (1937) Postlarval development of the coral Fungia actiniformis var. palawensis Doderlein. Palao Trop Biol Stat Stud 1:73–93

    Google Scholar 

  • Abe N (1939) Ecological studies on Rhizopsammia minuta var. mutsuensis Yabe and Eguchi. In: Jubilee publication for Prof H Yabe’s 60th birthday, vol 1. Japan Society for the Promotion of Scientific Research, Tokyo, pp 175–187

  • Achituv Y, Benayahu Y, Haniania J (1992) Planulae brooding and acquisition of zooxanthellae in Xenia macrospiculata (Cnidaria: Octocorallia). Helgol Wiss Meeresunters 46:301–310

    Google Scholar 

  • Atoda K (1951) The larva and postlarval development of the reef-building corals. J Morphol 89:1–15

    Google Scholar 

  • Avian M, Boero F, Mills C, Rossi L, Rottini-Sandrini L (1995) Cnidaria, Ctenophora. In: Minelli A, Ruffo S, La Posta S (eds) Checklist delle specie della fauna italiana. Edizioni Calderini, Bologna, pp 1–38

  • Babcock R (1990) Reproduction and development of the blue coral Heliopora coerulea (Alcyonaria: Coenothecalia). Mar Biol 104:475–481

    Google Scholar 

  • Babcock RC, Heyward AJ (1986) Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5:111–116

    Article  Google Scholar 

  • Babcock RC, Bull G, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394

    Article  Google Scholar 

  • Babcock RC, Wills BL, Simpson CJ (1994) Mass spawning of corals on a high latitude coral reef. Coral Reefs 13:161–169

    Google Scholar 

  • Beauchamp KA (1993) Gametogenesis, brooding and planulation in laboratory populations of a temperate scleractinian coral Balanophyllia elegans maintained under contrasting photoperiod regimes. Invertebr Reprod Dev 23:171–182

    Google Scholar 

  • Benayahu Y (1989) Reproductive cycle and developmental processes during embryogenesis of Clavularia hamra (Cnidaria, Octocorallia). Acta Zool 70:29–36

    Google Scholar 

  • Benayahu Y, Loya Y (1983) Surface brooding in the Red Sea soft coral Parerythropodium fulvum fulvum (Forskal, 1775). Biol Bull (Woods Hole) 165:353–369

    Google Scholar 

  • Benayahu Y, Weil D, Kleinman M (1990) Radiation of broadcasting and brooding patterns in coral reef Alcyonaceans. In: Hoshi M, Yamashita O (eds) Advances in invertebrate reproduction, vol 5. Elsevier, Amsterdam, pp 323–328

  • Cairns SD (1999) Species richness of recent Scleractinia. Atoll Res Bull 459:1–12

    Google Scholar 

  • Cairns SD, Hoeksema BW, Van Der Land J (1999) Appendix: list of extant stony corals. Atoll Res Bull 459:13–46

    Google Scholar 

  • Chia FS, Crawford BJ (1973) Some observations on gametogenesis, larval development and substratum selection of the sea pen Ptilosarcus guerneyi. Mar Biol 23:73–82

    Google Scholar 

  • Connell JH, Keough MJ (1985) Disturbance and patch dynamics of subtidal marine animals on hard substrata. In: Pickett STA, White PS (eds) The ecology of natural disturbance and patch dynamics. Academic, Orlando, pp 125–151

  • Dahan M, Benayahu Y (1998) Embryogenesis, planulae longevity, and competence in the octocoral Dendronephthya hemprichi. Invertebr Biol 117:271–280

    Google Scholar 

  • Diah Permata W, Kinzie III RA, Hidaka M (2000) Histological studies on the origin of planulae of the coral Pocillopora damicornis. Mar Ecol Prog Ser 200:191–200

    Google Scholar 

  • Edmondson CH (1929) Growth of Hawaiian corals. Bernice P Bishop Mus Bull 58:1–38

    Google Scholar 

  • Edmondson CH (1946) Behavior of coral planulae under altered saline and thermal conditions. Bernice P Bishop Mus Occ Pap 18:283–304

    Google Scholar 

  • Fadlallah YH (1981) The reproductive biology of three species of corals from central California. PhD thesis, University of California, Santa Cruz

  • Fadlallah YH (1983a) Sexual reproduction, development and larval biology in scleractinian corals: a review. Coral Reefs 2:129–150

    Google Scholar 

  • Fadlallah YH (1983b) Population dynamics and life history of a solitary coral, Balanophyllia elegans, from central California. Oecologia 58:200–207

    Google Scholar 

  • Fadlallah YH, Pearse JS (1982) Sexual reproduction in solitary corals: overlapping oogenic and brooding cycles, and benthic planulas in Balanophyllia elegans. Mar Biol 71:223–231

    Google Scholar 

  • Fan TY, Dai CF (1998) Sexual reproduction of the scleractinian coral Merulina ampliata in southern Taiwan. Bull Mar Sci 62:897–904

    Google Scholar 

  • Fautin DG (2002) Reproduction of Cnidaria. Can J Zool 80:1735–1754

    Google Scholar 

  • Fautin DG, Spaulding JG, Chia FS (1989) Cnidaria. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates. 4A. Fertilization, development, and parental care, chap 2. Wiley, Chichester, pp 43–62

  • Glynn PW, Gassman NJ, Eakin CM, Cortes J, Smith DB, Guzman HM (1991) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Galapagos Islands (Ecuador). I. Pocilloporidae. Mar Biol 109:355–368

    Google Scholar 

  • Glynn PW, Colley SB, Gassman NJ, Black K, Cortés J, Maté JL (1996) Reef coral reproduction in the eastern Pacific: Costa Rica, Panamá, and Galapagos Islands (Ecuador). III. Agariciidae (Pavona gigantea and Gardineroseris planulata). Mar Biol 125:579–601

    Google Scholar 

  • Glynn PW, Colley SB, Ting JH, Maté JL, Guzman HM (2000) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama and Galapagos Islands (Ecuador). IV. Agariciidae, recruitment and recovery of Pavona varians and Pavona sp. a. Mar Biol 136:785–805

    Google Scholar 

  • Goffredo S, Telò T (1998) Hermaphroditism and brooding in the solitary coral Balanophyllia europaea (Cnidaria, Anthozoa, Scleractinia). Ital J Zool 65:159–165

    Google Scholar 

  • Goffredo S, Zaccanti F (2004) Laboratory observations of larval behavior and metamorphosis in the Mediterranean solitary coral Balanophyllia europaea (Scleractinia, Dendrophylliidae). Bull Mar Sci 74:449–458

    Google Scholar 

  • Goffredo S, Telò T, Scanabissi F (2000) Ultrastructural observations of the spermatogenesis of the hermaphroditic solitary coral Balanophyllia europaea (Anthozoa, Scleractinia). Zoomorphology 119:231–240

    Google Scholar 

  • Goffredo S, Arnone S, Zaccanti F (2002) Sexual reproduction in the Mediterranean solitary coral Balanophyllia europaea (Scleractinia, Dendrophylliidae). Mar Ecol Prog Ser 229:83–94

    Google Scholar 

  • Goffredo S, Mattioli G, Zaccanti F (2004a) Growth and population dynamics model of the Mediterranean solitary coral Balanophyllia europaea (Scleractinia, Dendrophylliidae). Coral Reefs 23:433–443

    Google Scholar 

  • Goffredo S, Mezzomonaco L, Zaccanti F (2004b) Genetic differentiation among populations of the Mediterranean hermaphroditic brooding coral Balanophyllia europaea (Scleractinia, Dendrophylliidae). Mar Biol 145:1075–1083

    Google Scholar 

  • Gutiérrez-Rodríguez C, Lasker HR (2004) Reproductive biology, development and planula behavior in the Caribbean gorgonian Pseudopterogorgia elisabethae. Invertebr Biol 123:54–67

    Google Scholar 

  • Hand C, Uhlinger (1992) The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol Bull (Woods Hole) 182:169–176

    Google Scholar 

  • Harii S, Omori M, Yamakawa H, Koike Y (2001) Sexual reproduction and larval settlement of the zooxanthellate coral Alveopora japonica Eguchi at high latitudes. Coral Reefs 20:19–23

    Google Scholar 

  • Harriott VJ (1983) Reproductive ecology of four scleractinian species at Lizard Island, Great Barrier Reef. Coral Reefs 2:9–18

    Google Scholar 

  • Harrison PL (1985) Sexual characteristics of scleractinian corals: systematic and evolutionary implications. In: Gabrié C, et al (eds) Proc 5th Int Coral Reef Congr, vol 4. Antenne Museum—EPHE, Moorea, French Polynesia, pp 337–342

  • Harrison PL (1988) Pseudo-gynodioecy: an unusual breeding system in the scleractinian coral Galaxea fascicularis. In: Choat JH, et al (eds) Proc 6th Int Coral Reef Symp, vol 2. Symposium Executive Committee, Townsville, pp 699–705

  • Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world. 25. Coral reefs. Elsevier, Amsterdam, pp 133–207

  • Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189

    Google Scholar 

  • Hartnoll RG (1977) Reproductive strategy in two British species of Alcyonium. In: Keegan BF, Ceidigh PO, Boaden PJS (eds) Biology of benthic organisms. Pergamon, New York, pp 321–328

  • Heltzel PS, Babcock RC (2002) Sexual reproduction, larval development and benthic planulae of the solitary coral Monomyces rubrum (Scleractinia: Anthozoa). Mar Biol 140:659–667

    Article  Google Scholar 

  • Hirose H, Kinzie III RA, Hidaka M (2000) Early development of zooxanthella-containing eggs of the corals Pocillopora verrucosa and P. eydouxi with special reference to the distribution of zooxanthellae. Biol Bull (Woods Hole) 199:68–75

    Google Scholar 

  • Hughes TP, Ayre D, Connell JH (1992) The evolutionary ecology of corals. Trends Ecol Evol 7:292–295

    Article  Google Scholar 

  • Kinchington D (1981) Organic-matrix synthesis by scleractinian coral larval and post-larval stages during skeletogenesis. In: Gomez ED, et al (eds) Proc 4th Int Coral Reef Symp, vol 2. Marine Sciences Center, University of the Philippines, Manila, pp 107–113

  • Kramarsky-Winter E, Loya Y (1998) Reproductive strategies of two fungiid corals from the northern Red Sea: environmental constraints? Mar Ecol Prog Ser 174:175–182

    Google Scholar 

  • Kruger A, Schleyer MH (1998) Sexual reproduction in the coral Pocillopora verrucosa (Cnidaria: Scleractinia) in Kwa Zulu-Natal, South Africa. Mar Biol 132:703–710

    Google Scholar 

  • Kruger A, Scleyer MH, Benayahu Y (1998) Reproduction in Anthelia glauca (Octocorallia: Xeniidae). I. Gametogenesis and larval brooding. Mar Biol 131:423–432

    Google Scholar 

  • Krupp DA (1983) Sexual reproduction and early development of the solitary coral Fungia scutaria (Anthozoa: Scleractinia). Coral Reefs 2:159–164

    Google Scholar 

  • Lacaze-Duthiers H (1873) Développment des coralliaires. Actinaires à Polypiers. Arch Zool Exp Gén 2:269–348

    Google Scholar 

  • Lacaze-Duthiers H (1897) Faune du Golfe du Lion. Coralliaires, Zooanthaires, Sclérodermés. Arch Zool Exp Gén 5:1–249

    Google Scholar 

  • Lei Y, Warrior R (2000) The Drosophila Lissencephaly1 (DLis1) gene is required for nuclear migration. Dev Biol 226:57–72

    Google Scholar 

  • Lyons KM (1973) Collar cells in the planula and adult tentacle ectoderm of the solitary coral Balanophyllia regia (Anthozoa, Eupsammiidae). Z Zellforsch 145:57–74

    Google Scholar 

  • Moseley HN (1881) On the deep sea Madreporaria. Report on the scientific results of the voyage of H.M.S. Challenger (1873–1876). Zoology 2:127–248

    Google Scholar 

  • Neves EG, Pires DO (2002) Sexual reproduction of Brazilian coral Mussimilia hispida (Verril, 1902). Coral Reefs 21:161–168

    Google Scholar 

  • Pianka ER (1970) On r- and K- selection. Am Nat 104:592–597

    Article  Google Scholar 

  • Richmond RH (1997) Reproduction and recruitment in corals: critical links in the persistence of reefs. In: Birkeland C (ed) Life and death of coral reefs. Chapman and Hall, New York, pp 175–197

  • 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

    Google Scholar 

  • Riechmann V, Ephrussi A (2001) Axis formation during Drosophila oogenesis. Curr Opin Genet Dev 11:374–383

    Google Scholar 

  • Shlesinger Y, Loya Y (1985) Coral community reproductive patterns: Red Sea versus the Great Barrier Reef. Science 228:1333–1335

    Google Scholar 

  • Shlesinger Y, Loya Y (1991) Larval development and survivorship in the corals Favia favus and Platygyra lamellina. Hydrobiologia 216/217:101–108

    Google Scholar 

  • Shlesinger Y, Goulet TL, Loya Y (1998) Reproductive patterns of scleractinian corals in the northern Red Sea. Mar Biol 132:691–701

    Google Scholar 

  • Soong K (1991) Sexual reproductive patterns of shallow-water reef corals in Panama. Bull Mar Sci 49:832–846

    Google Scholar 

  • Stimson JS (1978) Mode and timing of reproduction in some common hermatypic coral of Hawaii and Enewetak. Mar Biol 48:173–184

    Google Scholar 

  • Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–54

    Google Scholar 

  • Szmant-Froelich A, Yevich P, Pilson MEQ (1980) Gametogenesis and early development of the temperate coral Astrangia danae (Anthozoa: Scleractinia). Biol Bull (Woods Hole) 158:257–269

    Google Scholar 

  • Szmant-Froelich A, Reutter M, Riggs L (1985) Sexual reproduction of Favia fragum (Esper): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico. Bull Mar Sci 37:880–892

    Google Scholar 

  • Tomascik T, Sander F (1987) Effects of eutrophication on reef-building corals. III. Reproduction of the reef-building coral Porites porites. Mar Biol 94:77–94

    Google Scholar 

  • Van Buskirk C, Schüpbach T (1999) Versatility in signaling: multiple responses to EGF receptor activation during Drosophila oogenesis. Trends Cell Biol 9:1–4

    Google Scholar 

  • Vaughan TW, Wells JW (1943) Revision of the suborders, families, and genera of the Scleractinia. Geol Soc Am Spec Pap 44:1–363

    Google Scholar 

  • Vermeij MJA, Sampayo E, Bröker K, Bak RPM (2004) The reproductive biology of closely related coral species: gametogenesis in Madracis from the southern Caribbean. Coral Reefs 23:206–214

    Google Scholar 

  • Waller RG, Tyler PA, Gage JD (2002) Reproductive ecology of the deep-sea scleractinian coral Fungiacyathus marenzelleri (Vaughan, 1906) in the northeast Atlantic Ocean. Coral Reefs 21:325–331

    Google Scholar 

  • Ward S (1992) Evidence for broadcast spawning as well as brooding in the scleractinian coral Pocillopora damicornis. Mar Biol 112:641–646

    Google Scholar 

  • Wells JW (1956) Scleractinia. In: Moore RC (ed) Treatise of invertebrate paleontology, part F. Coelenterata. University of Kansas Press, Lawrence, pp F328–F444

  • Willis BL, Babcock RC, Harrison PL, Oliver JK, Wallace CC (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. In: Gabrié C, et al (eds) Proc 5th Int Coral Reef Congr, vol 4. Antenne Museum—EPHE, Moorea, French Polynesia, pp 343–348

  • Wilson HV (1888) On the development of Manicina aereolata. J Morph 2:191–282

    Google Scholar 

  • Yonge CM (1932) A note on Balanophyllias regia, the only eupsammiid coral in the British fauna. J Mar Biol Assoc UK 28:219–224

    Google Scholar 

  • Zibrowius H (1980) Les scléractiniaires de la Méditerranée et de l’Atlantique nord-oriental. Mem Inst Oceanogr (Monaco) 11:1–284

    Google Scholar 

Download references

Acknowledgements

We wish to thank E. Manzardo, S. Arnone, M. Pasquini, L. Tomesani, M. Longagnani, L. Podda and O. Panaro for their valuable SCUBA assistance in collecting monthly samples. Coral photographs are by G. Neto. R. Falconi gave us valuable suggestions on earlier drafts of this paper, as well as assistance in defining laboratory guidelines. O. Langmead (Marine Biological Association of the United Kingdom) revised and significantly improved this paper. We also thank two anonymous reviewers for their valuable revision. M. Cesarini and E. Boschieri assisted in the layout of the histological photographs and plates. The Marine Science Group (http://www.marinesciencegroup.org) gave us scientific, technical and logistical support. Bologna Scuba Team gave us logistical support for the dives. Our research was supported by the Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR), by the Associazione dei Tour Operator Italiani (ASTOI) and by Scuba Schools International Italy (SSI). The experiments complied with the current laws of Italy.

Author information

Authors and Affiliations

  1. Department of Evolutionary and Experimental Biology, Alma Mater Studiorum—University of Bologna, Via F. Selmi 3, 40126, Bologna, Italy

    S. Goffredo, J. Radetić, V. Airi & F. Zaccanti

Authors
  1. S. Goffredo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Radetić
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. Airi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Zaccanti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. Goffredo.

Additional information

Communicated by R. Cattaneo-Vietti, Genova

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goffredo, S., Radetić, J., Airi, V. et al. Sexual reproduction of the solitary sunset cup coral Leptopsammia pruvoti (Scleractinia: Dendrophylliidae) in the Mediterranean. 1. Morphological aspects of gametogenesis and ontogenesis. Marine Biology 147, 485–495 (2005). https://doi.org/10.1007/s00227-005-1567-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-005-1567-z

Keywords

Search

Navigation