Lobe Variation in <I>Sinularia Nanolobata</I> Verseveldt, 1977 (Cnidaria: Alcyonacea)

BULLETIN OF MARINE SCIENCE, 63(1): 229–240, 1998 CORAL REEF PAPER

LOBE VARIATION IN SINULARIA NANOLOBATA VERSEVELDT, 1977 (CNIDARIA: ALCYONACEA)

Y. Benayahu

ABSTRACT Colonies of Sinularia were collected on the reef flat off south Patong, Phuket, Thai- land. The lobes in some of the colonies occur in two forms: (1) those composed of relatively large, spherical or flattened lobules, here termed “normal lobes”, and (2) those highly divided into many small, rough surfaced lobules, here termed “aberrant lobes”. The survey revealed that colonies at least 40 cm across were formed of lobes of both morphologies, while smaller colonies were formed only from normal lobes. Regardless of lobe morphology, all specimens collected have similar sclerite characteristics, and were identified as S. nanolobata Verseveldt, 1977, family Alcyoniidae. This species ap- pears to be characterized by intra-specific lobe variation, and such observed intra-colony lobe variation is presented for an octocoral species for the first time. It is speculated that the aberrant lobes might be a result of abnormal regeneration of damaged areas of the colonies as a response either to predation, or some adverse environmental conditions encountered by large colonies in the course of their life span. The aberrant lobes reflect part of the variation of the operational species and emphasize the need to consider total colony morphology during taxonomic practice, and also to assess the ranges of intra- specific variation among alcyoniid octocorals.

Soft corals of the family Alcyoniidae Lamouroux, 1812 represent a highly diverse group consisting of 18 genera with a wide morphological variation (Alderslade, 1983; Verseveldt and Bayer, 1988). Their generic diagnoses are based on morphological features both of colonies and sclerites (e.g., Verseveldt and Bayer, 1988). The genus Sinularia May, 1898 of the Alcyoniidae has been diagnosed as “colonies with distinct stalk, polyparium thrown into folds, lobes or digitate processes; sclerites spindles or clubs” (Versevedt and Bayer, 1988). Within this genus, species identification relies on colony morphology, mainly features of the lobes and sclerite architecture (Verseveldt, 1980). To date, Sinularia com- prises over 120 species distributed throughout the entire Indo-Pacific region (Verseveldt, 1980, 1983a; Li, 1982; Verseveldt and Benayahu, 1983; Alderslade, 1987; 1994; Alderslade and Baxter, 1987; Alderslade and Shirwaiker, 1991, Malyutin, 1990, van Ofwegen and Benayahu, 1992; van Ofwegen and Vennam, 1991, 1994; Benayahu, 1993, 1995). Sinularia species are a major faunistic component on many coral reefs, where they often form aggregates and monopolize large reef areas (Benayahu, 1985, 1995). Ranges of intra-specific morphological variation of either the sclerites or the colonies have only been described for some species of Sinularia; e.g., S. leptoclados (Ehrenberg, 1834) and S. variabilis Tixier-Durivault, 1945 [Verseveldt, 1980], S. gardineri (Pratt, 1903) [Verseveldt and Benayahu, 1983], S. capitalis (Pratt, 1903), S. flexibilis (Quoy and Gaimard, 1883), S. hirta (Pratt, 1903) and S. muralis May, 1899 [van Ofwegen and Vennam, 1994]. For numerous species, the existing literature presents descriptions of the type specimens only (e.g., Verseveldt, 1980), and offers no data on their intra-specific variation. No attempt has been made so far to illustrate morphological variation within different parts of the same Sinularia colony, or in any other alcyoniid. Many Sinularia colonies are long lived and attain large sizes, >40 cm in diameter (pers. observ.), and for practical

229 230 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 1, 1998 reasons, only small colonies or fragments of larger ones are usually collected in the field. Consequently, most descriptions of Sinularia species are not based on full size specimens (e.g., Verseveldt, 1980), and therefore allow only a very limited assessment of possible intra-colony variation. The present study deals with morphological variation in a Sinularia species. It reports for the first time variation in lobe morphology in different parts of the same colony. Likewise, it describes intraspecific variation among colonies occurring in the same reef habitat. Although the causes of the phenomenon are only speculated upon, the signifi- cance of the current findings to the taxonomy of species of Alcyoniidae is considered.

MATERIALS AND METHODS

An extensive soft coral survey was conducted during the UNESCO sponsored First Octocoral Research Workshop and Advanced Training Course, held at the Phuket Marine Science Center, Thailand, 30 November–13 December, 1987 (Alderslade et al., 1989). Aggregates of Sinularia colonies were observed on the reef flat off South Patong, Phuket, during this survey. Most of the large colonies possessed patches of lobes with a vastly different morphology from the neighboring areas. Four fragments, each comprising the two different lobe forms, were collected from four different colonies. In addition, two other specimens were removed from smaller adjacent colonies which had only one lobe style. The specimens were preserved in 70% alcohol and deposited at the Zoological Museum of Tel Aviv University (ZMTAU), Israel. Various colonies were photographed underwater with a Nikonos III camera and close up attachment. Small portions of the different lobes forms (1.5 × 1.5 cm) were removed from the collected specimens, and decalcified in a mixture of 1:1 formic acid (50%) and sodium citrate (15%) for 40 min. Then they were sectioned with a scalpel, and examined under a binocular dissecting microscope (x100) for the possible presence of encysted organisms. Sclerites were obtained by dissolv- ing the organic tissues with 10% sodium hypochlorite, and were prepared for scanning electron microscopy by rinsing with double distilled water and drying at room temperature. The sclerites were then gold coated, and examined with a Jeol JSM 840A scanning electron microscope operated at 25 kv.

RESULTS

All six specimens were confirmed as Sinularia nanolobata Verseveldt, 1977, by a comparison with the holotype, RMNH Coel. no. 11840, during a visit to the National Mu- seum of Natural History, Leiden, The Netherlands (August, 1993).

Sinularia nanolobata Verseveldt, 1977 (Figs. 1–6)

Sinularia nanolobata Verseveldt, 1977: 305–307, fig. 2, pl. 2.

Material.—ZMTAU Co 28621, fragments of six colonies, reef flat, South Patong, Phuket, Thailand, 2 December 1987, Y. Benayahu . Description.—All the specimens have an encrusting growth form, with diameters as follows: 17 × 15 (Fig. 1A), 9 × 8 (Fig. 1B), 9 × 5, 13 × 9, 18 × 8, and 12 × 11 cm. They have a thin flat base, which in some cases extended beyond the point of attachment. Four specimens were sampled from colonies that had two distinct types of lobes: (1) those BENAYAHU: LOBE VARIATION IN SINULARIA 231

Figure 1. Sinularia nanolobata Verseveldt, 1977 (ZMTAU Co 28621), a. Part of a colony with normal lobes and aberrant lobes (arrows), b. Part of a colony with aberrant lobes, c. A close up of aberrant lobes. Scale at 1a, 10 mm, refers to 1a-b, scale at 1c, 20 mm. 232 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 1, 1998

Figure 2. Sinularia nanolobata Verseveldt, 1977, underwater photographs, a. Scars between normal lobes (arrows), b. Aberrant lobes with coarse surface, c. Aberrant lobes adjacent to normal lobes, d. Aberrant lobes with papillate surface. Scale at 2a, 10 mm, applies to 2a–d.

composed of relatively large, spherical or flattened lobules (Fig. 1A, outer region), here termed “normal lobes”, and (2) those highly divided into many small, rough surfaced lobules, (Fig. 1A, inner region, and Fig. 1B,C), here termed “aberrant lobes”. Within the colonies, the aberrant lobes are very prominent and mostly appear as complex protuberances up to 20 cm in diameter. They are surrounded by normal lobes, with no morphological gradation between the two forms (Fig. 1A). A close-up of the aberrant lobes is given in Figure 1C; the tiny surface-elevations, 1–1.4 mm high, bear the polyp openings. Within areas of normal lobes, bright scars were sometimes observed (Fig. 2A). Both the preserved specimens (Fig. 1A,C) and the living colonies (Fig. 2B–D) show that the morphology of the aberrant lobes is not consistent. In some instances, individual lobes or lobules can be recognized within the protuberances, despite their rough surface (Figs.1A, 2B,C), while in others there are clusters of papillae with no distinct lobe-structure (Figs. 1B,2D). Two of the specimens collected have only normal lobes. A survey on the reef indicated that only large colonies, >40 cm in diameter, possess the aberrant lobes, while all smaller colonies have only normal lobes. In all of the preserved specimens the polyps are retracted. Examination of the decalcified aberrant lobes did not reveal infection of the tissue, or the polyp cavities, by encysted organisms. BENAYAHU: LOBE VARIATION IN SINULARIA 233

Figure 3. Sinularia nanolobata Verseveldt, 1977 (ZMTAU Co 28621), sclerites from the surface of the lobes. Scale at 3a, 0.01 mm, applies to 3a–o.

Comparison between the sclerites of specimens with only normal lobes and those that also have aberrant lobes, indicated complete agreement in all respective parts of the colonies. The surface layer of both normal and aberrant lobes contains clubs, 0.10–0.20 mm long (Fig. 3). Some have a central wart (Figs. 3A,D,H–J,M), and the others have wide and warty heads. Their handles are more or less pointed and bear a few warts. The surface of the scars (Fig. 2A) has similar sclerites. In the surface layer of the base there are also 234 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 1, 1998

Figure 4. Sinularia nanolobata Verseveldt, 1977 (ZMTAU Co 28621), sclerites from the surface of the stalk. Scale at 4a, 0.01 mm, applies to 4a–i.

clubs (Figs. 4,5), 0.09–0.20 mm long. Some possess wide warty heads (Figs. 4G,H,L, 5A,B), and the handles bear warts that are sometimes very coarse (Figs. 4G,5B,I). The interior of both lobe forms and of the base contain thick spindles (Fig. 6), 1.3–2 mm long, with pointed or rounded ends (Fig. 6A-F,H), and a few have a side branch (Fig. 6G). The tubercles are simple and spaced, with a diameter of 0.010–0.022 mm (Fig. 6I). There are no polyp sclerites. Color.—In alcohol the colonies are light cream. BENAYAHU: LOBE VARIATION IN SINULARIA 235

Figure 5. Sinularia nanolobata Verseveldt, 1977 (ZMTAU Co 28621), sclerites from the surface of the stalk. Scale at 5a, 0.01 mm, applies to 5a–l. 236 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 1, 1998

Figure 6. Sinularia nanolobata Verseveldt, 1977 (ZMTAU Co 28621), sclerites from the interior of the lobes and the base. Scale at 6a, 0.1 mm, applies to 6a-g; scale at 6i, 0.01 mm, only applies to 6i.

Remarks.—There is a full agreement with the sclerites of the type of S. nanolobata Verseveldt, 1977 and the examined material. However, the type has only the normal lobes and none of the aberrant ones. Field notes.—The species occurred on the reef flat in aggregates composed of numerous colonies which were sometimes as large as 1–2 m across. The colonies were light brown yellowish. Geographical distribution.—The holotype was collected in the Molluccas. This new material extends the species range to Phuket, Andaman Sea. BENAYAHU: LOBE VARIATION IN SINULARIA 237

DISCUSSION

This study demonstrates lobe variation in S. nanolobata collected at South Patong, Phuket, Thailand. On the reef there were colonies with either normal lobes, as described for the type specimen (Verseveldt, 1977), or colonies with both normal and aberrant lobes, recorded here for the first time. The sclerites of the respective parts of the two lobe forms are identical, and the sclerites of all specimens examined are in complete agreement with those described for the holotype. The present findings indicate that the lobes of S. nanolobata display morphological variation within individual colonies and amongst colonies of the same aggregate, thus leading to both an intra-colony and intra-specific lobe variation in a Sinularia species. Often many species, particularly those with a sessile mode of life, such as scleractinian corals, present a wide range of morphologies in response to habitat differences (refer- ences in: Miller, 1994, Veron, 1995). This makes species identification a task for special- ists and gives rise to much of confusion in the taxonomic literature (Veron, 1995). The failure to recognize intra-specific variation among alcyoniids, has resulted in some taxonomic literature presenting obscure differences between described species. These cir- cumstances have prompted subsequent revisions of some of the most common and diverse reef-inhabiting alcyoniid genera, e.g., Sinularia, Sarcophyton and Lobophytum (Verseveldt, 1980, 1982, 1983b), resulting in the discovery of numerous invalid synonyms. They highlighted for the first time ranges of intra-specific variation for reef alcyoniids. However, none of these revisions has raised the feasibility of an intra-colony variation among alcyoniids. Presence of aberrant lobes in S. nanolobata raises the unavoidable question: are they malformed or do they comprise part of the full variation of the species? Among scleractinian corals, intra-colony morphological differences are well recognized (Veron, 1995) and might be expressed as corallite variation or the presence of two different morphologies within a single colony. Also in these corals, some intra-colony variation has been attrib- uted to skeletal malformations, which have been previously described in several species as neoplasms or tumors (Squires, 1965; Cheney, 1975; Loya et al., 1984; Peters et al., 1986). However, suspected cases of neoplasms in deep-sea corals have been reinterpreted as galls caused by ascothoracid crustaceans (Grygier and Cairns, 1996). This controversy illustrates the uncertainty about the nature and the causes of such intra-colony skeletal variation. As far as octocorals are concerned, there is no reported evidence for intra- colony morphological variation in the entire group. This is excluding some species with growth malformations resembling galls, as found in the Gorgoniidae, Gorgonia ventalina (Morse et al., 1977), and in the Plexauridae, Pseudoplexaura spp (Goldberg et al., 1984), P. porosa, P. flagellosa, P. wagenaari and Plexaura flexuosa (Botero, 1990). These galls are associated with pathogenic filamentous green algae that induce production of skeletal capsules (Goldberg, 1984). Absence of encysted organisms in the aberrant lobes of S. nanolobata in part rules out the possibility of such a stimulus for their development. Unfortunately, the tissue of the specimens was not adequately preserved for histological sectioning, so the possible presence of causative agents such as algae, bacteria or fungi still awaits future examination. The scars found on some colonies of S. nanolobata (Fig. 2A) might be a result of the activity of corallivores. Predation upon octocorals (e.g., Sammarco and Coll, 1992), in- cluding some Sinularia species (e.g., Wylie and Paul, 1989; Van Alstyne et al., 1992), has 238 BULLETIN OF MARINE SCIENCE, VOL. 63, NO. 1, 1998

been documented. Similarly, adverse external physical forces such as wave action or sedi- ment abrasion can cause similar tissue damage in soft corals (pers. observ.). So, it is a possibility that the aberrant lobes of S. nanolobata might result from abnormal regeneration of damaged areas. At this stage it can be postulated that the aberrant lobes reflect part of the intra-specific variation of S. nanolobata, yet the exact cause for this variation and its relation to colony size still remains to be shown. As opposed to scleractinian corals as well as gorgoniid and plexaurid octocorals (see above), alcyoniid species tend to contract dramatically and thus change their shape after being collected or preserved. But, the underwater photographs of S. nanolobata supply direct evidence that intra-colony variation in the lobes of this species is undoubtedly a natural characteristic. The similarity in the shape and dimensions of the sclerites found in the normal and the aberrant lobes implies that only the soft tissues contribute to the observed differences. Examination of only small fragments of Sinularia colonies without consideration of the whole colonies may underestimate the morphological ranges described for a given species. The results of this study indicate that such variation is seem- ingly to be found in alcyoniid colonies that may encounter in course of their history the causes that can lead to such phenomenon. Yet, it still remains to determine the potential of alcyoniid species to alter their morphology and respond to various environmental param- eters. Similarly, it remains to be shown whether the observed variability is genetically derived. Such information is essential for assessing the boundaries of variation of the different species in order to facilitate accurate taxonomic investigations.

ACKNOWLEDGMENTS

I would like to express my gratitude to D. Troost (UNESCO-Paris), J. R. E Harger and M. Marani (Unesco-ROSTSEA) for sponsoring the Unesco/Comar First Octocoral Research Workshop and Advance Training Course Phuket, Thailand. Special thanks are due to H. Chansang (PMBC) for her enthusiasm and support that were behind the success of the Workshop. My sincere thanks to K. Muzik and P. Alderslade for their friendship and endless efforts that made the Workshop a success. I am indebted to all the participants of the Workshop and the staff members of the PMBC for their help. I express my profound gratitude to F. M. Bayer and P. Alderslade for their comments and constructive criticism on the draft of this paper. I am obliged to L. P. van Ofwegen and J. C. Den Hartog for their assistance during my visit at the Nationaal Natuurhistorisch Museum, Leiden, The Netherlands. I wish to thank F. Scanerani for valuable assistance with scanning electron microscopy, A. Shoob for photography, and A. Shlagman for curatorial skills.

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DATE SUBMITTED: March 22, 1996. DATE ACCEPTED: July 31, 1996.

ADDRESS: Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, 69978 Tel Aviv, Israel. E-mail: [email protected].