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Sexual Reproduction of the Solitary Sunset Cup Coral Leptopsammia Pruvoti (Scleractinia: Dendrophylliidae) in the Mediterranean

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Sexual Reproduction of the Solitary Sunset Cup Coral Leptopsammia Pruvoti (Scleractinia: Dendrophylliidae) in the Mediterranean Marine Biology (2005) 147: 485–495 DOI 10.1007/s00227-005-1567-z RESEARCH ARTICLE S. Goffredo Æ J. Radetic´Æ V. Airi Æ F. Zaccanti Sexual reproduction of the solitary sunset cup coral Leptopsammia pruvoti (Scleractinia: Dendrophylliidae) in the Mediterranean. 1. Morphological aspects of gametogenesis and ontogenesis Received: 16 July 2004 / Accepted: 18 December 2004 / Published online: 3 March 2005 Ó Springer-Verlag 2005 Abstract Information on the reproduction in scleractin- came indented, assuming a sickle or dome shape. We can ian solitary corals and in those living in temperate zones hypothesize that the nucleus’ migration and change of is notably scant. Leptopsammia pruvoti is a solitary coral shape may have to do with facilitating fertilization and living in the Mediterranean Sea and along Atlantic determining the future embryonic axis. During oogene- coasts from Portugal to southern England. This coral sis, oocyte diameter increased from a minimum of 20 lm lives in shaded habitats, from the surface to 70 m in during the immature stage to a maximum of 680 lm depth, reaching population densities of >17,000 indi- when mature. Embryogenesis took place in the coelen- viduals mÀ2. In this paper, we discuss the morphological teron. We did not see any evidence that even hinted at aspects of sexual reproduction in this species. In a sep- the formation of a blastocoel; embryonic development arate paper, we report the quantitative data on the an- proceeded via stereoblastulae with superficial cleavage. nual reproductive cycle and make an interspecific Gastrulation took place by delamination. Early and late comparison of reproductive traits among Dend- embryos had diameters of 204–724 lm and 290–736 lm, rophylliidae aimed at defining different reproductive respectively. When released, the larvae had completed strategies. The present study on L. pruvoti is the first in- ontogenesis and swam by a ciliary movement with the depth investigation of the reproductive biology of a aboral pole at the anterior, their shape varied from species of this genus. As expected for a member of the spherical to cylindrical (in the latter the oral–aboral axis family Dendrophylliidae, L. pruvoti is a gonochoric and measured 695–1,595 lm and the transversal one mea- brooding coral. The gastrodermal tissue of the gameto- sured 267–633 lm). genetic mesenteries we examined was swollen and granular, which led us to hypothesize that interstitial cells could have a trophic function favoring gameto- genesis. Undifferentiated germ cells arose in the gastro- dermis and subsequently migrated to the mesoglea, Introduction where they completed gametogenesis. During spermary development, spermary diameter increased from a min- Sexual reproduction, which entails the dispersal of imum of 14 lm during the immature stages to a maxi- genetically unique larval recruits, plays a crucial role in mum of 410 lm during the mature stages. As oogenesis the life cycle and guarantees the survival and evolution progressed, we observed a gradual reduction in the nu- of the community (Harrison and Wallace 1990; Hughes cleus to cytoplasm ratio due to the steady synthesis of et al. 1992). Information on sexual reproduction is yolk. During the final stages of oogenesis, after having essential to understanding genetic structure and popu- migrated to the extreme periphery of the oocyte and lation connectivity and their effects on population having firmly adhered to the oolemma, the nucleus be- dynamics, as well as to understanding the resistance and resilience of populations vis a` vis natural and anthro- pogenic disturbances (Connell and Keough 1985). Basic Communicated by R. Cattaneo-Vietti, Genova data includes sexuality (hermaphroditic or gonochoric), S. Goffredo (&) Æ J. Radetic´Æ V. Airi Æ F. Zaccanti reproductive mode (broadcasting or brooding), embry- Department of Evolutionary and Experimental Biology, onic and larval development. Alma Mater Studiorum—University of Bologna, Studies to date on sexual reproduction in scleractin- Via F. Selmi 3, 40126 Bologna, Italy E-mail: stefano.goff[email protected] ians have been almost exclusively on tropical and sub- Tel.: +39-051-2094244 tropical colonial corals (Fadlallah 1983a; Harrison et al. Fax: +39-051-2094286 1984; Shlesinger and Loya 1985; Szmant 1986; Harrison 486 and Wallace 1990; Richmond and Hunter 1990; Rich- Lion, near Marseilles. The author reported sex-sepa- mond 1997). In most cases, reproduction is character- rated individuals and embryonic development within the ized by hermaphroditism and broadcasting, and by an coelenteron of females. annual gametogenic cycle that ends with a short period We are currently studying sexual reproduction in during which germ cells are released into the environ- L. pruvoti living in the eastern Ligurian Sea near Leg- ment. Temperature, photoperiod, tides and lunar phases horn. We are conducting morphological, cyto-histo- seem to play a role in synchronizing gametogenic pro- metric and quantitative studies on the gametogenesis, cesses. embryonic development and larval stages of these We do not have much information on temperate organisms, as well as genetic and population dynamics scleractinians (Beauchamp 1993; Harii et al. 2001; studies (manuscripts in preparation). The studies being Heltzel and Babcock 2002). Aside from recent work by conducted on L. pruvoti are part of a broader research Goffredo et al. (2002, and references therein), studies framework that we have developed to fill the gaps in our from the Mediterranean basin date back to the 19th knowledge of the biology of Mediterranean scleractin- century, to the work of Lacaze-Duthiers (1873, 1897). ians (Goffredo and Telo` 1998; Goffredo et al. 2000, Finally, as noted by Heltzel and Babcock (2002), most 2002, 2004a, 2004b; Goffredo and Zaccanti 2004). In this studies focus on colonial corals, leaving a lack of paper we describe morphological aspects of spermato- knowledge on solitary species. Given the importance of genesis, oogenesis, embryogenesis and larval develop- reproduction and recruitment to survival recovery fol- ment in L. pruvoti. In a separate paper, we will report on lowing disturbances, and for the broader conservation quantitative data regarding the annual reproductive and management of scleractinian species, widening our cycle, including the size of individuals at sexual matu- knowledge would help us to construct a database that rity, sex ratio, the cyto-histometric analyses of gameto- would allow comparisons of different life-strategy genesis, a comparison of gonadal development with adaptations in scleractinians, as well as between solitary environmental parameters, seasonality in sexual devel- and colonial organisms in general (Harrison and Wal- opment and planulation, and fecundity. lace 1990). Dendrophylliidae is a cosmopolitan taxon of colonial or solitary corals, comprising 148 extant species divided into 19 genera (Avian et al. 1995; Cairns 1999; Cairns Materials and methods et al. 1999). There are seven species of Dendrophylliidae living in the Mediterranean today, subdivided into five Polyps of Leptopsammia pruvoti were collected at Cala- genera, two of which, Balanophyllia and Leptopsammia, furia (Leghorn; 43°28.4¢N; 10°20¢E) in 18 monthly are solitary. Systematics of these two genera is not clear, samplings from July 2001 to December 2002. Divers some authors consider them to be synonymous (Balan- took samples at depths of 15–17 m (see Goffredo et al. ophyllia=Leptopsammia in Vaughan and Wells 1943; 2004a for a description of the habitat and topography of Wells 1956; Fadlallah 1983a; Heltzel and Babcock the sampling area). 2002), while others argue that they are two separate taxa We made sure that the samples, made up of 12 (Zibrowius 1980; Cairns et al. 1999). We agree with specimens each, included the entire size range of the Cairns et al. (1999) and their most recent list of extant population (1–8 mm maximum diameter of the oral species of Scleractinia, in which Leptopsammia and disc). Biometric analyses were performed in the field; Balanophyllia are recorded as two distinct taxa. length (L, maximum diameter of the oral disc), width (l, According to Cairns et al. (1999), the genus Leptop- minimum diameter of the oral disc) and height (h, oral– sammia comprises ten species, geographically distributed aboral diameter of the polyp) were measured. Volume in the Atlantic, Indian and central-western Pacific (V) was calculated using the formula: Oceans. There is only one species, Leptopsammia pruvoti V ¼ h à ðÞÃL=2 ðÞÃl=2 p ð1Þ Lacaze-Duthiers, 1897, living in the Mediterranean (Avian et al. 1995). L. pruvoti has also been reported (after Goffredo et al. 2002). along Atlantic coasts from Portugal to southern Eng- Specimens were then fixed and transferred to the land. Along the species’ distributional area, the mean laboratories for histological analysis. After decalcifica- annual sea surface temperature ranges from 12°C, in tion and dehydration, the polyps were embedded in southern England, to 19°C, in the Mediterranean. This paraffin and serial transverse sections were cut at 7-lm species tends to live in shaded habitats, under overhangs intervals from the oral to the aboral poles. and in grottos, at depths ranging from the surface to Histological observations of gametogenesis and 70 m (Zibrowius 1980). The species reaches an average embryogenesis were made under a light microscope. population density of 4,000–17,000 individuals mÀ2 at Cyto-histological readings were made with a LEICA depths ranging between 15 and 21 m (authors’ personal Q5001 W image analyzer. We measured the maximum observations). There is not much information on the and minimum diameters of the spermaries and of the biology of this species. The only data available con- oocytes in nucleated sections. The size of each repro- cerning reproduction dates back >100 years (Lacaze- ductive element was determined as the average of the Duthiers 1897) from samples collected in the Golfe du two diameters. In accordance with earlier studies on 487 gametogenesis in scleractinians by Beauchamp (1993), the mesogleal envelope. We identified five developmental Kramarsky-Winter and Loya (1998), Kruger and stages: Schleyer (1998), Glynn et al.
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