Sexual reproductive cycle of the epibiotic soft coral Alcyonium coralloides (Octocorallia, Alcyonacea)

AQUATIC BIOLOGY Aquat Biol Vol. 18: 113–124, 2013 doi: 10.3354/ab00493 Published online April 3 INTRODUCTION Competition for substrate space is a key factor de - termining the survival of benthic species such as octo corals (Connell 1961, Pequegnat 1964, Paine 1974, Jackson 1977). Due to this dependence on the colonization of stable substrates (Gili & Coma 1998), octocorals have developed mechanisms and strategies allowing them to successfully compete for the available substrate (Jackson 1977). Epibiosis is a biological relationship consisting of a non-parasitic or - ga nism spending at least 1 phase of its life cycle growing on a larger organism (Wahl 1989). This strategy is adopted by many species in highly structured and diversified benthic communities where competition for space is vital, as in Mediterranean coralligenous formations (Ros et al. 1985, Witman & Dayton 2001). Coralligenous formations are produced mainly by the accumulation of encrusting calcareous or coral - line algae (Fredj & Laubier 1985, Ballesteros 2006). Octocoral species such as Paramuricea clavata (Risso, 1826), Eunicella cavolinii (Kock, 1887), E. singularis (Esper, 1791), E. verrucosa (Pallas, 1766) and Corallium rubrum (Linnaeus, 1758) and soft coral genera such as Alcyonium are important architectural com- © Inter-Research 2013 · www.int-res.com*Email: [email protected] Sexual reproductive cycle of the epibiotic soft coral Alcyonium coralloides (Octocorallia, Alcyonacea) Elena Quintanilla1,*, Josep-Maria Gili1, Pablo J. López-González2, Georgios Tsounis1,4, Teresa Madurell1, Ida Fiorillo1, Sergio Rossi3 1Institut de Ciències del Mar, ICM-CMIMA (CSIC), 08003 Barcelona, Spain 2Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, 41012 Sevilla, Spain 3Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallés, Spain 4Present address: Department of Ecology, Leibniz Center for Tropical Marine Ecology, 28359 Bremen, Germany ABSTRACT: Alcyonium coralloides is an epibiotic soft coral overgrowing living colonies of Mediterranean gorgonians. The main features of the sexual reproductive cycle of this soft coral species are described and quantified for the first time, in a population found at 18 to 22 m depth off the Medes Islands (NW Mediterranean). A. coralloides is a gonochoric internal brooder. The sexual cycle showed a single reproductive event per year. Gametogenesis took 5 to 6 mo, which is the shortest known gametogenesis in littoral octocorals (especially for oogenesis). The maximum mean ± SD diameter was 365 ± 86 µm for spermatic cysts and 632 ± 125 µm for mature oocytes. Sperm was released in spring (late May). Average male and female fecundity in this last phase of the cycle was 15 ± 9 spermatic cysts and 7 ± 4 oocytes per polyp, respectively. Larvae of about 1000 µm in length were observed in the gastrovascular cavities of female colonies in May, before they were released in June. We suggest that the remarkable short gametogenesis and timing shown by A. coralloides is an adaptation to optimize the colonization of its host (in this case the gorgonian octocoral Paramuricea clavata). We conclude that A. coralloides larvae could be ready to settle in early summer when the host P. clavata is probably more vulnerable as a result of its own reproductive cycle coming to an end. KEY WORDS: Alcyonium coralloides .Paramuricea clavata · Epibiosis · Reproductive effort · Soft corals · Reproductive coupling · Gametogenesis Resale or republication not permitted without written consent of the publisher FREEREE ACCESSCCESS Aquat Biol 18: 113–124, 2013 ponents of the coralligenous assemblages, increasing their biodiversity and complexity (Gili & Ros 1984, Wendt et al. 1985, Sebens 1991, Tsounis et al. 2006). These organisms are highly vulnerable to environmental perturbations because their slow growth rates, low recruitment, sessile life form and exposed structural colonial forms imply slow recovery rates (Coma et al. 2004). Disturbances of anthropogenic origin include injuries due to contact with fishing lines, anchors or SCUBA divers that may result in decreased fecundity and increase opportunities for colonization by epibionts (Bavestrello et al. 1997, Tsounis et al. 2012). Furthermore, partial mortalities due to persistent heat waves may be an advantage for new settlers in the denuded skeletons (Cerrano et al. 2000). The octocoral (Cnidaria, Anthozoa) Alcyonium coral loides (Pallas, 1766) is an epibiont species that grows by fouling (‘runner’ type) the apical axis of (most likely injured) colonies of gorgonians such as Paramuricea clavata, Eunicella singularis, E. cavo li nii, E. verrucosa and Leptogorgia sarmentosa (Esper, 1789) (McFadden 1999, McFadden et al. 2001). The ‘runner’ type morphology consists of building encrusting tissue networks that show low physical resistance and a large area of tissue to the organism that horizontally colonizes a surface (Jackson 1979). The soft coral indirectly adopts a 3-dimensional morphology by exploiting the arboreal morphology of the gorgonian host species. The water flow is greater with in - creasing distance from the substrate (Butman 1987). Thus, having a 3-dimensional morphology and a distal position on the branches of gorgonians can be a trophic advantage for the epibiont. Exposure to higher water flow enhances both passive suspension feeding and evacuation of metabolic waste of colo nies (Boero 1987, Wahl 1989). Thus, an epibiotic habit provides this soft coral with a favourable hydro dynamic position that confers greater volumetric water flow and more efficient suspension feeding (Best 1988). The reproductive pattern is the main feature de - scribing the life strategy of a species. For the first time, we describe the main quantitative parameters of the sexual reproductive cycle of Alcyonium coral - lo ides and compare them to those of other littoral octo coral species. The genus Alcyonium presents a wide diversity of patterns in the mode of reproduction and sexuality (McFadden et al. 2001, Kahng et al. 2011). However, little is known about the sexual reproduction of these anthozoans, which play an essential role in benthic communities (Gili & Coma 1998, Fautin 2002). We also investigated the implications of the epibiotic lifestyle of A. coralloides on its reproductive pattern. We hypothesized that the relatively simple colonial structure and reproductive strategy shown by A. coralloides (and other encrusting organisms) might be evolutionarily favoured due to its lower energetic needs when growing on other erect substrata (in the case of A. coralloides, the branches of Paramuricea clavata and other gorgonians). We argue that the ecological advantage of epibiont species in highly structured and diversified benthic communities can also be expressed in their reproductive pathway. MATERIALS AND METHODS Alcyonium coralloides samples were cut from colonized branches of Paramuricea clavata off Cova de la Vaca, within the Marine Protected Area of the Medes Islands (NW Mediterranean, 42°03’N, 3°15’E) be - tween 18 and 22 m depth. The sampling site is a large tunnel connecting 2 sides of one of the islets, and harbours a population of P. clavata. The abundance of A. coralloides is higher in this tunnel than usually found in other populations of P. clavata, due to the impact of SCUBA diving tourists that injure the corals, which thus favours colonization by A. coralloides (Tsounis et al. 2012). The tunnel is among the major SCUBA attractions along the Costa Brava and receives about 70000 visitors per yr (Lloret 2003, Coma et al. 2004). Nine sampling trips were carried out by SCUBA diving between March 2008 and March 2009, usually monthly when weather conditions allowed the fieldwork. Twenty colony fragments of Alcyonium coralloides growing on the same number of colonies of Paramuricea clavata were collected in each sampling trip, yielding a total of 180 samples in the whole sampling period of this study. All samples were immediately fixed in buffered formalin (4% in seawater). The collected colonies of A. coralloides were about 10 mm wide (coenenchyme covering the dead gorgonian axis) and ca. 50 mm long. We tried to sample the smallest fragments possible of A. coralloides , al - ways from the apical part of the gorgonian branches, to minimize impact. Sampling was haphazard; however, because not many colonies were left to be sampled in the tunnel, we had to sample tissue from the same individuals repeatedly over time. The colour pattern of Alcyonium coralloides colonies agrees with that described by Weinberg (1977) and morphotype M1 described by McFadden (1999): the sclerites of the coenenchyme were red, yellow in the tentacles and proximal part of the 114 Quintanilla et al.: Alcyonium coralloides reproductive cycle 115 polyp, and red in the distal part of the polyp (Fig. 1a,b). Variability in colour patterns might exist, since white and pink colonies have been reported from deeper waters (Groot & Weinberg 1982). A total of 900 po lyps (5 polyps per collected colony) were opened to count and measure reproductive products (oocytes and spermatic cysts). The sampling effort, representing the minimum significant sample size for the number of colonies and polyps in males and females that had to be removed, was the same as that used in other studies on reproduction in Mediterranean octocorals (e.g. Coma et al. 1995). Sex determination was carried out by direct observation of reproductive products and confirmed by subsequent histological sections. Oocytes were yellow and firm, whereas male spermatic cysts were white and relatively fragile to manipulation. A binocular stereomicroscope (×20) was used for measuring the diameter of the oocytes and spermatic cysts. Polyps were dissected by removing the anthocodia to expose the gastrovascular cavity. The dissected polyps were chosen haphazardly. In each po - lyp, the diameter of the sexual products was counted and measured. The average diameter (minimum detection size 50 µm) and the average fecundity (number of oocytes or spermatic cysts per polyp) were obtained per sex and month. The size–frequency distributions of reproductive-product diameters and their average volume, measured as a sphere (µm3 polyp−1), were also analysed. Temperature data (20 m depth) were obtained from the meteorological station of l’Estartit every 3 to 4 d. In order to detect and monitor gametogenic and embryonic development, selected samples from both sexes in all sampled months were prepared for histological observations. Fragments were decalcified in a solution of 10% formic acid for a few minutes, rinsed in running water to remove excess acid in the tissues, dehydrated in a gradient of ethyl alcohols and then embedded in paraffin. Histological sections 6 to 8 µm thick were stained with Ramón y Cajal’s Triple Stain (Gabe 1968). RESULTS Sexual cycle Alcyonium coralloides is gonochoric, with all po - lyps of a colony of the same sex. Larvae were found inside polyps of female colonies in May 2008 (Fig. 1c). Although the reproductive cycle was an nual, gametogenesis lasted only 5 to 6 mo. Based on presence and subsequent absence of larvae from May to June, larval release was inferred. However, spermatic cysts were present in May (Fig. 2a) in the gastrovascular cavities of male colonies. The maximum monthly (mean ± SD) spermatic cyst diameter observed was 365 ± 86 µm, and 632 ± 125 µm for mature oocytes in female colonies (Fig. 2). Both maximum values occurred in May, the last month of the gametogenic cycle. Also in this month fecundity (mean ± SD) was 15 ± 9 spermatic cysts polyp−1 in male colonies, and 7 ± 4 oocytes polyp−1 in females (Fig. 3). Gametogenic cycle Spermatic cysts and oocytes showed an annual cycle of development, with internal fertilization of Fig. 1. (a) Colony of the epibiont Alcyonium coralloides on a branch of Paramuricea clavata. (b) Polyp from a male colony with spermatic cysts and (c) larvae of a female colony collected in May 2008 Aquat Biol 18: 113–124, 2013 the oocytes and release of larvae in May. In both sexes, generation and development of reproductive products took 5 to 6 mo, probably beginning in December (no samples available) and ending with the release of sperm and larvae in May. In both males and females, the first evidence of small reproductive products (0−100 µm) was found in January, possibly marking the onset of oogenesis in the previous month (Figs. 4 & 5). Reproductive products of intermediate size classes (300−400 µm) were also present in fe - males, but smaller sizes were found in males (100−200 µm). In male colonies, the diameter (mean ± SD) of spermatic cysts increased by 34% between March 2008 (240 ± 95 µm) and May 2008 (365 ± 86 µm), just prior to the release of male sexual products (Fig. 2a). In January 2009, the first spermatic cysts were detected, with a diameter of 91 ± 36 µm; they achieved a final diameter of 311 ± 97 µm in March 2009 (Fig. 2a). No spermatic cysts were found in samples between June and November 2008. Polyp fecundity decreased from (mean ± SD) 34 ± 15 to 15 ± 9 spermatic cysts polyp−1 between March and May 2008, but increased 56% between January and March 2009 (13 ± 11 and 30 ± 13 spermatic cysts polyp−1, respectively; Fig. 3a). The average oocyte diameter in female colonies doubled in size over 2 mo, from 304 ± 105 µm in March 2008 to 632 ± 125 µm in May 2008 (Fig. 2b). During June, July, August and November of 2008, no oocytes were found in female colonies. In January 2009, the average size of oocytes was 191 ± 66 µm, increasing 60% up to 475 ±113 µm in March 2009 (Fig. 2b). The fecundity decreased by 46% in March and May 2008, whereas the highest fecundity was observed during January 2009 (16 ± 9 oocytes polyp−1) and then decreased by 15% (13 ± 7 oocytes polyp−1 in March 2009; Fig. 3b). The average volume (µm3polyp−1) of spermatic cysts and oocytes (Fig. 6) increased with development; the average diameter of both sexes followed the same pattern. Temperature was registered be - tween March 2008 and March 2009 (Fig. 7). The histological study showed that gametogenesis probably started in December: all male and female 116 Fig. 2. Alcyonium coralloides. Diameter (mean ± SD) of (a) spermatic cysts and (b) oocytes in samples collected during 2008 and 2009 Fig. 3. Alcyonium coralloides. Fecundity (mean ± SD) of (a) male and (b) female colonies collected during 2008 and 2009 Quintanilla et al.: Alcyonium coralloides reproductive cycle colonies sampled in November lacked reproductive products, whereas in the following sampled month (January), previtellogenic oocytes between 50 and 70 µm (Fig. 8b) and vitellogenic oocytes with in - creasing amount of lipid drops in the ooplasm (Fig. 8c,d) were present. Starting in January, male colonies showed spermatic cysts, which were present in all inspected male colonies in the following months. Spermatic cysts showed numerous heads of developing sperm and a thinner mesogleal envelope than oocytes (Fig. 9). Male colonies examined at the end of the cycle (May) were heterogeneous; the gastro vascular cavities of some colonies were completely empty (indicating the emission of spermatic cysts or sperm), whereas others still had some completely mature spermatic cysts full of sperm. Oocytes increased in size until May, when a few oocytes (some devoid of their mesogleal cover, and others still inside meso gleal capsules) but mainly larvae (showing epidermis with columnar cells and disaggregated internal yolk granular reserves) were observed in the gastrovascular cavities of polyps of female colonies. 117 0 10 20 30 40 50 60 70 March 2008 N = 1445 0 10 20 30 40 50 60 70 April 2008 N = 1316 0 10 20 30 40 50 60 70 May 2008 N = 588 0 10 20 30 40 50 60 70 January 2009 N = 396 0 10 20 30 40 50 60 70 0–100 Frequency (%) Diameter (µm) 101–200 201–300 301–400 401–500 501–600 601–700 701–800 801–900 901–1000 March 2009 N = 1474 Fig. 4. Alcyonium coralloides. Distribution of spermatic cyst diameter (µm) frequencies in male colonies collected during 2008 and 2009. N: total number of spermatic cysts measured per month 0 10 20 30 40 50 60 70 March 2008 N = 637 0 10 20 30 40 50 60 70 April 2008 N = 509 0 10 20 30 40 50 60 70 May 2008 N = 331 0 10 20 30 40 50 60 70 January 2009 N = 751 0 10 20 30 40 50 60 70 0–100 101–200 201–300 301–400 401–500 501–600 601–700 701–800 801–900 901–1000 March 2009 N = 449 Frequency (%) Diameter (µm) Fig. 5. Alcyonium coralloides. Distribution of oocyte dia - meter (µm) frequencies in female colonies collected during 2008 and 2009. N: total number of oocytes measured per month Aquat Biol 18: 113–124, 2013 DISCUSSION Similar to several other Alcyonium species (6 out of 12, according to Kahng et al. 2011), A. coralloides is a gonochoric species (Groot & Weinberg 1982). Gonochorism is the most common reproductive strategy in Octocorallia (70% according to Kahng et al. 2011), while hermaphroditism is the most common pattern among tropical scleractinian hexacorals (Har ri son & Wallace 1990, Kahng et al. 2011). A. coralloides is considered an internal brooder, and thus is characterized by internal fertilization and retention of larvae in the gastrovascular cavity of the polyps (Giese & Pearse 1974, McFadden et al. 2001). Internal brooding is the most common strategy among Alcyonium species (Kahng et al. 2011), whereas broadcast spawning is most common in tropical soft corals (Alino & Coll 1989, Cordes et al. 2001, Hwang & Song 2007, Kahng et al. 2011), and surface brooders are not common (Hwang & Song 2007, Kahng et al. 2011, Fiorillo et al. 2013). Gametogenesis Alcyonium coralloides showed an annual reproductive cycle, characterized by fast gametogenic de - velopment of similar duration for both sexes and an early release of larvae in spring (probably completing it in late May since larvae were absent in the samples from June). Our data revealed a shorter cycle (by 2 mo) in A. coralloides than that observed in other Alcyonium species and Mediterranean littoral octocorals (Table 1, Kahng et al. 2011). However, because variability of the reproductive cycle may oc - cur due to local or regional environmental conditions (e.g. temperature, food availability, other biological variables), more than 1 yr of observations is needed to support these results. Weinberg (1977) observed small oocytes (as eggs in his study) in speci mens of A. coralloides (as Parerythropodium corallo ides) collected in November, whereas Lacaze-Duthiers (1900) (as Sympodium coralloïdes) mentioned May to July as the reproductive period, and Lo Bianco (1909, as cited by Weinberg 1977) obtained larvae in the aquarium in June. Gametogenesis of male and female colonies had similar duration (5 to 6 mo), and oogenesis was shorter than that of other octocorals. In fact, the general tendency in octocorals is an oogenesis that lasts longer than spermatogenesis (Bena yahu & Loya 1984, 1986, Benayahu et al. 1990). This is also the general tendency among scleractinian hexacorals (Harrison & Wallace 1990, Harrison 2011) and is explained by the fact that oogenesis requires more time and energy than spermatogenesis because these lecitotrophic species develop ma ture oocytes with a great amount of yolk. These re serves will be the source of energy for sustaining larval development (Vance 1973). For instance, oogenesis in Mediterranean gorgonians such as Eunicella singularis, Leptogorgia sarmentosa and Paramuricea clavata 118 6.0 × 107 5.0 × 107 4.0 × 107 3.0 × 107 2.0 × 107 1.0 × 107 0.0 × 107 Volume spermatic cysts (µm3 polyp–1)Volume oocytes (µm3 polyp–1) 2.5 × 108 2.0 × 108 1.5 × 108 1.0 × 108 0.5 × 108 0.0 × 108 Mar 08 Apr 08 May 08 Jun 08 Jul 08 Aug 08 Sep 08 Oct 08 Nov 08 Dec 08 Jan 09 Feb 09 Mar 09 b a Fig. 6. Alcyonium coralloides. Volume for (a) total spermatic cyst content per polyp (male colonies) and (b) total oocyte content per polyp (female colonies) of samples collected during 2008 and 2009 10 15 20 25 Temp (°C) Mar 08 Apr 08 May 08 Jun 08 Jul 08 Aug 08 Sep 08 Oct 08 Nov 08 Dec 08 Jan 09 Feb 09 Mar 09 Fig. 7. Water temperature (°C) at 20 m depth between March 2008 and March 2009 Quintanilla et al.: Alcyonium coralloides reproductive cycle lasts 13 to 17, >12 and 13 to 18 mo, respectively, whereas spermatogenesis lasts 5 to 7 mo (Table 1). This trend is also characteristic in the soft coral Alcyonium acaule in the same area, with oogenesis and spermatogenesis lasting for 12 to 13 mo (Fiorillo et al. 2013; Table 1). In encrusting soft corals, this trend also appears in species such as Rhytisma fulvum fulvum (Forskål, 1775) (Parerythropodium fulvum fulvum; Benayahu & Loya 1983), in which oogenesis lasts 10 to 11 mo, while spermatogenesis lasts 7 to 9 mo. Our results also showed an increase in average volume of spermatic cysts and oocytes with a concurrent decrease in average fecundity during gametogenic development. This could be partially explained by absorption of the smallest generated sexual products in favour of the development of other spermatic cysts and oocytes that subsequently end their gametogenic cycle (Fiorillo et al. 2013). 119 Fig. 8. Alcyonium coralloides. Histological sections of female colonies: (a) retracted polyp with oocytes in the gastrovascular cavity, (b) previtellogenic oocyte ca. 50 µm in diameter, (c) vitellogenic oocytes with the ooplasm increasing in drops of yolk, (d) oocyte (mature or close to maturity), still inside mesogleal capsule, (e) mature oocyte free in the gastrovascular cavity, without parental mesogleal capsule, (f) interior of a gastrovascular cavity showing a group of larvae with diverse amount of disaggregating reserves, and an oocyte still in its mesogleal capsule, (g) detail of the epithelia of adjacent larvae, showing typical columnar epidermis and a thin mesogleal layer separating it from their incipient gastrodermis Aquat Biol 18: 113–124, 2013 Release of male sexual products The synchronization of both sexes in the release of sexual products is a common trend among broadcastspawning octocorals that allows maximizing the fertilization success (Alino & Coll 1989). This synchroni - zation is promoted by external factors such as temperature (Grigg 1977) and lunar cycle (Brazeau & Lasker 1989, 1990). In subtropical alcyonaceans, the release of male gametes coincides with increased water temperature in late spring (e.g. Eunicella singula ris, Paramuricea cla va ta, Sarcophyton glaucum (Quoy & Gaimard, 1833), Alcyonium acaule Linnaeus, 1758; see Coma et al. 1995, Benayahu & Loya 1986, Ribes et al. 2007, Fiorillo et al. 2013). In the case of E. singularis, male gametes are released in May to June, fertilization is internal, and release of larvae occurs in June to July (Ribes et al. 2007). The re lease 120 Fig. 9. Alcyonium coralloides. Histological sections of male colonies: (a) early spermatic cysts, without clear distinct lumen and disorganized spermaries, (b) developing spermatic cyst with typical lumen and future sperm flagellae and head of immature sperm still rounded and radially arranged, (c) developing spermatic cyst showing all maturation stages of the sperm heads, from rounded bodies (on the periphery of the cyst; bottom of the image), more concentrated (centre of the image) and fully defined and mature sperm heads, distinctly triangular and strongly stained (in the most internal parts of the cyst; upper part of the image), (d) interior of a gastrovascular cavity of a colony collected in April, showing spermatic cysts in different stages of development (sperm heads at the bottom of the image are strongly stained, denoting an advanced stage of maturation), (e) two adjacent spermatic cysts from a colony collected in April, showing the asynchrony in the development of cysts (the one on the left is fully developed, with disorganized sperm heads reaching the parental mesogloeal capsular layer, while the one on the right still contains rounded immature sperm heads) Quintanilla et al.: Alcyonium coralloides reproductive cycle 121 of sperm in A. coralloides oc curs from mid-May on, while the oocytes are retained in the female polyp for internal ripening and fertilization. This release of sperm coincides with a 2° increase in water temperature (from 14.8 to 16.7°C be tween 14 and 21 May 2008, Fig. 7), but it appears to precede spawning in other Alcyonium species and Medi terranean octo corals (see Table 1). Release of larvae In octocorals, less than 1 wk is en - ough for the transition from zygote to planula (Alino & Coll 1989, Babcock 1990, Gutierrez-Rodríguez & Lasker 2004). Internal fertilization and planulae development might occur in a short period, as is the case of Paramuricea clavata, in which blastulae de veloped in 24 h and planulae ap - peared after 48 to 72 h (Linares et al. 2008). As mentioned above, the re - lease of Alcyonium coralloides larvae probably occurs in May to early June (larvae were completely absent in samples collected in June (see Figs. 2b, 3b, 5, & 6b). Although un known for the majority of octocoral species, some anthozoan larvae are already competent 2 h after release, whereas other larvae require several days (Atoda 1947, Harii & Kayanne 2003). Thus, it is plausible that larvae of A. coralloides are ready to settle on naked segments of P. clavata axes if these are available. Denudation can occur through biological (depredation by gastropod molluscs, e.g. Simnia and Coralliophilia species; Crocetta & Spanu 2008) or environmental causes (mortality events and diseases linked to climate warming; see Cerrano et al. 2000, Linares et al. 2008, Coma et al. 2009, Garrabou et al. 2009) or due to physical damage (e.g. excessive SCUBA diving activities in particular areas, fishing nets and lines; see Harmelin & Marino - poulos 1994, Tsounis et al. 2012), as occurred at our study site. Species Study site Sexuality Reproductive mode Cycle (mo) Spawning or breeding Cohorts Alcyoniidae Alcyonium acaule NE Mediterranean Sea Gonochoric Surface brooder 12−13 (M and F) July 2 F Alcyonium coralloidesa NW Mediterranean Sea Gonochoric Internal brooder 6−7 (M and F) Mid-May−June Alcyonium digitatum Man Island (N Atlantic) Gonochoric Broadcast spawner 12−13 (F) December−January Alcyonium glomeratum Atlantic and Mediterranean Sea Gonochoric Broadcast spawner Alcyonium hibernicum Man Island (N Atlantic) Parthenogenic Internal brooder 12 (F) Late summer (1−2 mo) Alcyonium pacificum Aleutian Islands Gonochoric Internal brooder July−August Alcyonium palmatum Mediterranean Sea Gonochoric Broadcast spawner August−October Alcyonium sidereum NW Atlantic Sea Hermaphroditic Internal brooder August Alcyonium sp. A Irish Sea Hermaphroditic Internal brooder Alcyonium sp. A3 Portugal Unknown Internal brooder Alcyonium sp. C San Juan Islands Unknown Internal brooder Alcyonium sp. M2 Mediterranean Sea Unknown Unknown Coraliidae Corallium rubrum NE Mediterranean Sea Gonochoric Internal brooder 24 (F), 12 (M) July−August 2 F Cornulariidae Cornularia cornucopiae NE Mediterranean Sea Parthenogenic Unknown 5 (F) August Gorgoniidae Eunicella singularis NE Mediterranean Sea Gonochoric Internal brooder 13−17 (F), 5−6 (M) May−July 2 F Leptogorgia sarmentosa NE Mediterranean Sea Gonochoric Broadcast spawner >12 (F) Late August−early September Plexauridae Paramuricea clavata NE Mediterranean Sea Gonochoric Surface brooder 13−18 (F), 6−7 (M) June−July 2 F aData from present study Table 1. Sexuality and mode of reproduction, length of reproductive cycle, season of the onset and duration of gamete proliferation, maturation and spawning or breeding, and cohorts for selected soft corals and gorgonian species from different geographic areas. F: female, M: male, blank cells: no data. Sources: Coma et al. (1995), Ribes et al. (2007), Rossi & Gili (2009), Kahng et al. (2011), Betti et al. (2012), Fiorillo et al. (2013)