Aggregations of a Sessile Ctenophore, Coeloplana sp., on Indo-West Pacific Gorgonians

Abstract

We document the benthic ctenophores Coeloplana sp. and Vallicula multiformis from Oman, extending their geographic range. A new Coeloplana species was found forming aggregations on gorgonians of two octocoral host genera, Melithaea and Euplexaura, representing associations previously unknown to occur in the Indo-West Pacific region. Our findings also illustrate the concurrent presence of the ectocommensal ophiuroid Ophiothela mirabilis, which adversely affects other Coeloplana species in the tropical West Atlantic, where it is considered invasive. This exploration contributes to our understanding of the biogeography, species distribution, and ectosymbiotic associations of these genera, setting the stage for a comprehensive species description and in-depth analysis of host relationships in future studies.

The realization that ctenophores are the sister group to all other Metazoa [1,2] and that many aspects of their biology are likely convergent with other phyla, is attracting attention to this small phylum. Ctenophores, commonly known as comb jellies, are most diverse, and thought to have originated in the plankton, but three lineages have taken up a benthic existence [1,2,3,4].

The order Platyctenida is the main group of benthic ctenophores, characterized by an expanded oral region that forms a creeping sole, loss of ctenes in the adults of most species, and extensive tentacles extended by flow for prey capture [5,6,7]. They predominantly exhibit two distinct body types: the “lyre-shaped” form, which has two large aboral projections to extend tentacles into the water column, and the “flat” form with oral-aboral compression.

Most platyctenes are ectosymbiont commensals that live in close association with cnidarians, echinoderms, and algae [6,7,8,9,10]. The number of individuals per host depends on the species, host, and environmental conditions and can vary from one to hundreds [7,8,11]. Brooding, paedogenesis, and fragmentation are the main modes of propagation. Hermaphroditism, larval dispersal, and rapid development are likely traits that promote colonization, sustain high population densities, and provide resilience [12]. They are consumed by various predators, including sea anemones, molluscs, brachyuran crabs, and fishes [8,13,14].

The order Platyctenida is currently divided into five families, with Coeloplanidae being the most diverse [15]. Coeloplanidae includes two genera, Coeloplana Kowlevsky, 1880, with about 35 species [15], one species in the West Atlantic, and the rest in the Indo-West Pacific region; and the monotypic Vallicula Rankin, 1956, recorded across all warm oceans (Figure 1). Recent molecular studies suggest that the genus Vallicula belongs to a different family (Bezio and Collins, pers. comm.). Coeloplana is differentiated by its flask-shaped tentacle sheaths from Vallicula, which has anchor-shaped (or H-shaped) sheaths with a prominent cross-piece [5]. Six species of Coeloplana have been reported from the northwestern Indian Ocean, one from the Persian Gulf [16] and Somalia [17], and five from the Red Sea [6,18] (Figure 1A,B). No coeloplanids have been previously recorded from Oman.

Identification of Coeloplanidae is based on colour pattern, patterns of aboral papillae, development of oral groove and oral lappets, and host [5,6,7,19]. Additionally, recent studies have utilized Cytochrome c Oxidase Subunit I (COI) sequences for species differentiation [10,18]. Vallicula multiformis is a habitat generalist with low host specificity, whereas most Coeloplana species are habitat specialists with high host specificity and are restricted to a specific host or a group of morphologically similar hosts [6,7,8,19].

This ectosymbiont/host association in coeloplanids can provide insights into species distributions and biogeography. Cnidarians are the most common hosts, with at least 19 described (and numerous undescribed) species of Coeloplana recorded from them, 17 obligately so. One species (C. loyai) lives on mushroom corals (Fungiidae), while the rest occur on octocorals, all but three on soft corals (Table 1). The only exceptions are the Atlantic C. waltoni and the Indo-West Pacific C. sophiae both known only from gorgonians, and the generalist C. duboscqui recorded from sea pens [6,7,12,20,21,22]. This suggests that soft-coral morphology is better suited for Coeloplana, and the low diversity of Coeloplana in the Atlantic compared to Indo-West Pacific reefs may be due to the practical absence of soft corals from Atlantic reefs [23]. Coeloplana species on gorgonians are generally also smaller than those on soft corals.

During a large-scale survey of the marine biodiversity of Oman (2019–2023) that aimed to characterize macroinvertebrate fauna, we encountered aggregations of an undescribed Coeloplana species on two gorgonian hosts, Melithaea Milne Edwards, 1857 (Melithaeidae) and Euplexaura Verrill, 1869 (Euplexauridae), around Masirah Island (Figure 1, Figure 2 and Figure 3, Videos S1 and S2). The animals were a few millimetres long and appeared to occupy the hosts without particular preference for location or orientation on the colony (Figure 2 and Figure 3). Approximately 15–30 individuals were found on Melithaea sp. colonies (Figure 2C,D), and over 60 individuals on Euplexaura sp. colonies (Figure 2A,B). They were noted in situ on Euplexaura colonies, but were cryptic on the orange-yellow Melithaea colonies and only noticed in the lab, when they crawled off the colony as water quality in their tank declined. Two colour forms, pink and yellow, cooccurred on both hosts and likely represent morphotypes of the same species. The yellow form is effectively invisible on the similar-coloured Melithaea (Figure 3). We reviewed all known species of Coeloplana and these specimens do not match any described species. In addition, we encountered Vallicula multiformis on a green alga host (Figure 4, Video S3).

The ctenophores co-occurred with the ectocommensal ophiuroid Ophiothela mirabilis (Verrill, 1867) (Figure 2B,C). This ophiuroid is invasive in the tropical West Atlantic and appears to negatively impact Coeloplana waltoni in south Florida [24].

Our observations constitute the first report of such aggregations on gorgonians in the Indo-West Pacific, as well as the first record of Coeloplana sp. and Vallicula multiformis in Oman. This discovery contributes to our understanding of ectosymbiont-host associations, biogeography, and species distribution of Coeloplana and Vallicula. Future research will focus on formally describing the species and its gorgonian hosts.

Figure 1. (A,B) Global distribution of Coeloplana (circles) and Vallicula (squares). Coeloplana records from octocoral hosts are purple in colour. The star represents the first record of the Coeloplana and Vallicula from Oman. (C) Locations of the observations and collections of Coeloplana sp. on gorgonian hosts in Masirah Island. Numbers indicate different species (Table 1, localities extracted from [6], and other publications). OM = Oman, PG = Persian Gulf, GO = Gulf of Oman, GA = Gulf of Aden, and RS = Red Sea. Blue shading in (B,C) represents depth.

Figure 1. (A,B) Global distribution of Coeloplana (circles) and Vallicula (squares). Coeloplana records from octocoral hosts are purple in colour. The star represents the first record of the Coeloplana and Vallicula from Oman. (C) Locations of the observations and collections of Coeloplana sp. on gorgonian hosts in Masirah Island. Numbers indicate different species (Table 1, localities extracted from [6], and other publications). OM = Oman, PG = Persian Gulf, GO = Gulf of Oman, GA = Gulf of Aden, and RS = Red Sea. Blue shading in (B,C) represents depth.

Table 1. List of valid species of Coeloplanidae and their host based on [6,15]. Please note that the octocoral taxonomy has been updated in the table as accurately as possible. The Coeloplana records from octocoral host have been shaded purple (corresponding to Figure 1).

Record No.	Species	Host
1a	C. agniae Dawydoff, 1930	Sclerophytum polydactylum (Octocorallia)
1b	C. agniae var. striata Dawydoff, 1938	Sclerophytum polydactylum (Octocorallia)
2	C. anthostella Song & Hwang, 2010	Dendronephthya spinulosa and other Dendronephthya spp. (Octocorallia)
3	C. astericola Mortensen, 1927	Echinaster luzonicus (Asteroidea)
4	C. bannwarthi Krambach, 1933	Diadema spp. (Echinoidea)
5	C. bocki Komai, 1920	Stereonephthya japonica, Dendronephthya spinulosa, D. dendricata (Octocorallia), Hydrozoa, algae, Echinodermata
6	C. duboscqui Dawydoff, 1930	Pteroides (Octocorallia), Hypnea (red algae)
7	C. echinicola Tanaka, 1932	Toxopneustes pileolus (Echinoidea)
8	C. fishelsoni Alamaru, Brokovich & Loya, 2015	Xenia umbellata, Paralemnalia (Octocorallia)
9a	C. gonoctena Krempf, 1920	Cladiella krempfi, Cladiella pachyclados (Octocorallia)
9b	C. gonoctena var. natalensis Pople, 1960	Cladiella krempfi (Octocorallia)
9c	C. gonoctena var. rosea Dawydoff, 1938	Klyxum (Octocorallia)
10	C. huchonae Alamaru, Brokovich & Loya, 2015	Dendronephthya hemprichi (Octocorallia)
11	C. indica Davansan &Varadarajan, 1942	NA
12	C. komaii Utinomi, 1963	Cladiella digitulata (Octocorallia)
13	C. krusadiensis Devanesen & Varadarajan, 1942	Pentaceros hedemanni (Asteroidea)
14	C. lineolata Fricke, 1970	Sarcophyton (Octocorallia)
15	C. loyai Alamaru & Brokovich, 2015	Herpolitha limax, Ctenactis echinata (Scleractinia)
16	C. mellosa Gershwin, Zeidler & Davie, 2010	Sarcophyton (Octocorallia)
17	C. mesnili Dawydoff, 1938	Planktonic/free living
18	C. meteoris Thiel, 1968	Free living on soft sediments
19	C. metschnikowii Kowalevsky, 1880	Zostera (seagrass)
20	C. mitsukurii Abbott, 1902	Melobesia (red algae) and Sargassum (brown algae)
21	C. perrieri Dawydoff, 1930	Posidonia (seagrass) or free living on rocks
22	C. punctata Fricke, 1970	Sarcophyton (Octocorallia)
23	C. reichelti Gershwin, Zeidler & Davie, 2010	Variety of red and green algae and seagrasses
24	C. scaberiae Matsumoto & Gowlett-Holmes, 1996	Scaberia agardhii (algae)
25	C. sophiae Dawydoff, 1938	Solenocaulon jedanensis (Octocorallia)
26	C. tattersalli Devanesen & Varadarajan, 1942	Planktonic/free living
27	C. thomsoni Matsumoto, 1999	Jania (coralline algae)
28	C. weilli Dawydoff, 1938	Heterocentrotus mamillatus (Echinoidea)
29	C. willeyi Abbott, 1902	Zostera, Caulerpa, Saragassum (seagrass and algae) and Echinothrix diadema, Echinothrix calamaris, Heterocentrotus mamillatus (Echinoidea)
30	C. waltoni Glynn, Bayer & Renegar, 2014	Various species of shallow-water gorgonians from the genera Eunicea, Plexaurella, Muricea, Gorgonia, Pseudoplexaura, Antillogorgia, Plexaura, Muriceopsis (Octocorallia)
31	C. wuennenbergi Fricke, 1970	Sarcophyton (Octocorallia)
32	C. yulianicorum Alamaru, Brokovich & Loya, 2015	Sarcophyton (Octocorallia)
33	Vallicula multiformis Rankin, 1956	Various algae and invertebrates, such as seagrasses, algae, Pearsonothuria graeffei (Holothuroidea)

Table 1. List of valid species of Coeloplanidae and their host based on [6,15]. Please note that the octocoral taxonomy has been updated in the table as accurately as possible. The Coeloplana records from octocoral host have been shaded purple (corresponding to Figure 1).

Record No.	Species	Host
1a	C. agniae Dawydoff, 1930	Sclerophytum polydactylum (Octocorallia)
1b	C. agniae var. striata Dawydoff, 1938	Sclerophytum polydactylum (Octocorallia)
2	C. anthostella Song & Hwang, 2010	Dendronephthya spinulosa and other Dendronephthya spp. (Octocorallia)
3	C. astericola Mortensen, 1927	Echinaster luzonicus (Asteroidea)
4	C. bannwarthi Krambach, 1933	Diadema spp. (Echinoidea)
5	C. bocki Komai, 1920	Stereonephthya japonica, Dendronephthya spinulosa, D. dendricata (Octocorallia), Hydrozoa, algae, Echinodermata
6	C. duboscqui Dawydoff, 1930	Pteroides (Octocorallia), Hypnea (red algae)
7	C. echinicola Tanaka, 1932	Toxopneustes pileolus (Echinoidea)
8	C. fishelsoni Alamaru, Brokovich & Loya, 2015	Xenia umbellata, Paralemnalia (Octocorallia)
9a	C. gonoctena Krempf, 1920	Cladiella krempfi, Cladiella pachyclados (Octocorallia)
9b	C. gonoctena var. natalensis Pople, 1960	Cladiella krempfi (Octocorallia)
9c	C. gonoctena var. rosea Dawydoff, 1938	Klyxum (Octocorallia)
10	C. huchonae Alamaru, Brokovich & Loya, 2015	Dendronephthya hemprichi (Octocorallia)
11	C. indica Davansan &Varadarajan, 1942	NA
12	C. komaii Utinomi, 1963	Cladiella digitulata (Octocorallia)
13	C. krusadiensis Devanesen & Varadarajan, 1942	Pentaceros hedemanni (Asteroidea)
14	C. lineolata Fricke, 1970	Sarcophyton (Octocorallia)
15	C. loyai Alamaru & Brokovich, 2015	Herpolitha limax, Ctenactis echinata (Scleractinia)
16	C. mellosa Gershwin, Zeidler & Davie, 2010	Sarcophyton (Octocorallia)
17	C. mesnili Dawydoff, 1938	Planktonic/free living
18	C. meteoris Thiel, 1968	Free living on soft sediments
19	C. metschnikowii Kowalevsky, 1880	Zostera (seagrass)
20	C. mitsukurii Abbott, 1902	Melobesia (red algae) and Sargassum (brown algae)
21	C. perrieri Dawydoff, 1930	Posidonia (seagrass) or free living on rocks
22	C. punctata Fricke, 1970	Sarcophyton (Octocorallia)
23	C. reichelti Gershwin, Zeidler & Davie, 2010	Variety of red and green algae and seagrasses
24	C. scaberiae Matsumoto & Gowlett-Holmes, 1996	Scaberia agardhii (algae)
25	C. sophiae Dawydoff, 1938	Solenocaulon jedanensis (Octocorallia)
26	C. tattersalli Devanesen & Varadarajan, 1942	Planktonic/free living
27	C. thomsoni Matsumoto, 1999	Jania (coralline algae)
28	C. weilli Dawydoff, 1938	Heterocentrotus mamillatus (Echinoidea)
29	C. willeyi Abbott, 1902	Zostera, Caulerpa, Saragassum (seagrass and algae) and Echinothrix diadema, Echinothrix calamaris, Heterocentrotus mamillatus (Echinoidea)
30	C. waltoni Glynn, Bayer & Renegar, 2014	Various species of shallow-water gorgonians from the genera Eunicea, Plexaurella, Muricea, Gorgonia, Pseudoplexaura, Antillogorgia, Plexaura, Muriceopsis (Octocorallia)
31	C. wuennenbergi Fricke, 1970	Sarcophyton (Octocorallia)
32	C. yulianicorum Alamaru, Brokovich & Loya, 2015	Sarcophyton (Octocorallia)
33	Vallicula multiformis Rankin, 1956	Various algae and invertebrates, such as seagrasses, algae, Pearsonothuria graeffei (Holothuroidea)

Figure 2. Aggregations of Coeloplana sp. on gorgonians around Masirah Island, Oman. (A,B) Colony of Euplexaura sp. at 18 m depth (BOMAN-13166) covered with both colour morphotypes of Coeloplana (red and yellow arrows), some with extended tentacles. (C,D) Colony of Melithaea sp. (BOMAN-13152) at 7 m depth. Coeloplana individuals occur in both colours in this species; however, it is very difficult to see them underwater. Note the concurrent presence of the ophiuroid O. mirabilis in both gorgonians (white arrows). All observations were made during the day (Photo credit: K. Samimi-Namin).

Figure 2. Aggregations of Coeloplana sp. on gorgonians around Masirah Island, Oman. (A,B) Colony of Euplexaura sp. at 18 m depth (BOMAN-13166) covered with both colour morphotypes of Coeloplana (red and yellow arrows), some with extended tentacles. (C,D) Colony of Melithaea sp. (BOMAN-13152) at 7 m depth. Coeloplana individuals occur in both colours in this species; however, it is very difficult to see them underwater. Note the concurrent presence of the ophiuroid O. mirabilis in both gorgonians (white arrows). All observations were made during the day (Photo credit: K. Samimi-Namin).

Figure 3. (A,B) Photographs of the two colour morphs of Coeloplana sp. (C,D) Close-ups of the aboral papillae (white arrow) (Photo credit: G. Paulay).

Figure 3. (A,B) Photographs of the two colour morphs of Coeloplana sp. (C,D) Close-ups of the aboral papillae (white arrow) (Photo credit: G. Paulay).

Figure 4. (A–C) Photographs of Vallicula multiformis from Oman (BOMAN-10006). (B,C) Close-ups of the same specimen showing the aboral sense organ (white arrow), papillae (red arrow), and the extension of the oral groove to the tentacle sheath (yellow arrow) (Photo credit: G. Paulay).

Figure 4. (A–C) Photographs of Vallicula multiformis from Oman (BOMAN-10006). (B,C) Close-ups of the same specimen showing the aboral sense organ (white arrow), papillae (red arrow), and the extension of the oral groove to the tentacle sheath (yellow arrow) (Photo credit: G. Paulay).