A New Species of Sea Anemone (Cnidaria: Anthozoa: Actiniaria) from Manus Basin Hydrothermal Vents, South-western Pacific

Please note that this is an author-produced PDF of an article accepted for publication following peer review. The definitive publisher-authenticated version is available on the publisher Web site 1 Marine Biology Research November 2005; 1(5) : 326 - 337 http://dx.doi.org/10.1080/17451000500380306 © 2005 Taylor & Francis The original publication is available at http://www.tandf.co.uk/journals/ Archimer http://www.ifremer.fr/docelec/ Archive Institutionnelle de l’Ifremer A new species of sea anemone (Cnidaria: Anthozoa: Actiniaria) from Manus Basin hydrothermal vents, South-western Pacific Pablo J. López-González1, Estefanía Rodríguez1,2, Michel Segonzac3* 1Biodiversidad y Ecología de Invertebrados Marinos, Departamento de Fisiología y Zoología, Facultad de Biología, Universidad de Sevilla, Sevilla, Spain e-mail: [email protected] 2Departamento de Biología Marina y Oceanografía, Instituto de Ciencias del Mar, CMIMA (CSIC), Paseo Marítimo de la Barceloneta, Barcelona, Spain e-mail: fan[email protected] 3Ifremer, Centre de Brest, DEEP-LEP/Centob, Plouzané, France *: Corresponding author : [email protected] Abstract: During the BIOACCESS Japanese cruises (1996 & 1998), active hydrothermalism and associated vent fauna were studied on the South-eastern Rift of Manus Basin (South-western Pacific). In the PACMANUS vent field, a conspicuous vent fauna was sampled, including an actinostolid sea anemone (Actiniaria) belonging to an undescribed genus and species. Pacmanactis hashimotoi gen. et spec. nov. is here described, and represents the 9th sea anemone reported from hydrothermal vents. Keywords: Actiniaria, Actinostolidae, hydrothermal vents, back-arc basins, Manus Basin Pacmanactis-Shinji-180205.doc A NEW SPECIES OF SEA ANEMONE (CNIDARIA: ANTHOZOA: ACTINIARIA) FROM MANUS BASIN HYDROTHERMAL VENTS, SOUTHWESTERN PACIFIC Pablo J. López-González1, Estefanía Rodríguez1, 2 & Michel Segonzac3 1: Biodiversidad y Ecología de Invertebrados Marinos, Departamento de Fisiología y Zoología, Facultad de Biología, Universidad de Sevilla, Reina Mercedes 6, 41012 – Sevilla, Spain (e-mail: [email protected]). 2: Departamento de Biología Marina y Oceanografía, Instituto de Ciencias del Mar, CMIMA (CSIC), Paseo Marítimo de la Barceloneta, 37-49, 08003 Barcelona, Spain (email: [email protected]). 3: Ifremer, Centre de Brest, DRO-EP/Centob, BP 70, 29280 Plouzané, France (e-mail: [email protected]). Key words: Actiniaria, Actinostolidae, hydrothermal vents, back-arc basins, Manus Basin, sea anemones. Abstract During the BIOACCESS Japanese cruises (1996 & 1998), active hydrothermalism and associated vent fauna were studied on the Southeastern Rift of Manus Basin (Southwestern Pacific). In the Pacmanus vent field, a conspicuous vent fauna was sampled, including an actinostolid sea anemone belonging to an undescribed genus and species. Pacmanactis hashimotoi gen. et spec. nov. is here described, and represents the ninth sea anemone reported from hydrothermal vents. 1 Introduction Eight species of sea anemones have been documented from hydrothermal vents. Six of them belong to the family Actinostolidae and two species belong to the family Hormathiidae (see Desbruyères & Segonzac, 1997; Fautin & Barber, 1999; LópezGonzález et al., 2003). From the Atlantic Ocean, the occurrence of two actinostolid species was pointed out: Parasicyonis ingolfi Calgren, 1942 and Maractis rimicarivora Fautin & Barber, 1999. From the Pacific Ocean, four actinostolid species have been reported (one of them identified only at generic level): Actinostola sp. [as Actinostola sp. in the text, but as Actinostola callosa (Verrill 1882) in the figure, see Doumenc & van Praët, 1988, fig. 1], Cyananthea hydrothermala Doumenc & Van-Praët, 1988, Marianactis bythios Faustin & Hessler, 1989 and Paranthosactis denhartogi LopezGonzalez et al., 2003. Actinostola callosa and C. hydrothermala were collected at East Pacific Rise (EPR) vents, 12º48’N-103º56’W, 2635 m, while M. bythios was sampled at Mariana back-arc basin 18º11’N-144º42.4’E, 3660 m, and P. denhartogi at Guaymas Basin, Gulf of California, 27°00.94’-111°24.66’W, 2025 m. To present, only two hormathiid species have been reported from hydrothermal vents, both from EPR-13°N: Chondrophellia coronata (Verrill, 1883) and Phelliactis sp. (Doumenc & Van-Praët 1988). In this paper, we describe a new genus and species of actinostolid collected during the two Japanese Cruises BIOACCESS’96 and BIOACCESS’98, at the hydrothermal vent area of PACMANUS, Pual Ridge, Bismark Sea in the SW Pacific, N of Papua New Guinea (Fig. 1). Fig. 1. Map indicating the hydrothermal (PACMANUS) vent where Pacmanactis hashimotoi gen. et spec. nov. described in this paper was collected. Material and Methods The seven specimens studied here were collected during the BIOACCESS’96 and ‘98 cruises organized by the Japan Agency for Marine-Earth Science and Technology (JAMSTEC) and conducted by Jun Hashimoto (Nagasaki University), on board the R/V Natsushima, equipped with the manned submersible Shinkai 2000, from 26 October to 29 November 1996 and 13 to 25 November 1998. The main goal of these cruises was the study of the composition, distribution, ecology and diversity of 2 hydrothermal vent fauna on PACMANUS (1700 m) and DESMOS (1900 m) sites of Manus Basin (Hashimoto et al. 1999, and Fig. 1). After recovery, the sea anemones were fixed in 10% seawater formalin, and then preserved in 70% ethanol. Fragments from selected specimens were dehydrated in buthanol (Johansen, 1940) and embedded in paraffin. Histological sections 7-8 µm thick were stained with Ramón y Cajal's Triple Stain (Gabe, 1968). Cnidae measurements were made from preserved material in squash preparations at 1000x magnification with Nomarski differential interference contrast optics. Frequencies given are subjective impressions based on squash preparations. The material studied in this article is deposited in the National Science Museum of Tokyo (NSMT), and the collection of the research team “Biodiversidad y Ecología de Invertebrados Marinos” of the Faculty of Biology at the University of Seville in Spain (BEIM). Results Phylum CNIDARIA Order ACTINIARIA Hertwig, 1882 Family ACTINOSTOLIDAE Carlgren, 1932 Pacmanactis gen. nov. Diagnosis.— Actinostolidae with well developed, adherent, and circular pedal disc. Column smooth, distal part including oral disc wider than mid-column and pedal disc, not divisible into scapus and scapulus.Sphincter distinctly marked distally as a prominent circumferential marginal ridge, relatively weak, mesogloeal, with wellisolated lacunae. Tentacles of uniform thickness along entire length. Inner tentacles longer than outer, with microbasic b-mastigophores basally. Longitudinal tentacle and oral disc circular musculature ectodermal; that of tentacles equally well developed on all sides. Mesenteries not arrayed according to Actinostola rule; first and second cycles of mesenteries perfect; all stronger ones fertile, including the directives. Two well developed siphonoglyphs and two pairs of directives. Retractor muscles diffuse; parietobasilar muscles not differentiated; basilar musculature differentiated. Mesogloea relatively thick. Same number of mesenteries distally and proximally. Cnidom: spirocysts, basitrichs, holotrichs, microbasic b-mastigophors, microbasic pmastigophores. Type species.— Pacmanactis hashimotoi spec. nov. Etymology and gender.— The generic name is derived from the type locality (PACMANUS) and the word –actis, a common suffix in actiniarian genera. The gender is feminine. Pacmanactis hashimotoi spec. nov. (Figures 2-6, table 1) Type material. Holotype: NSMT, BIOACCESS’98 cruise, dive 1075, 22 Nov. 1998, SW Pacific, Manus Basin (N of Papua New Guinea), hydrothermal vent area 3 PACMANUS, Field D, Barnacles site, 03843.60?S-151840.32?E, 1674 m, 1 specimen partially dissected and histological slides. Paratypes: MNHN, with the same sampling data as the holotype, 1 specimen; NSMT, with the same sampling data as the holotype, 2 specimens. Additional material. BEIM, 2 specimens, BIOACCESS’98 cruise, PACMANUS (sample M 13, field E), with the same sampling data as the type material; NSMT, 1 specimen, BIOACCESS’96 cruise, dive 913, 3. Nov. 1996, SW Pacific, Manus Basin, PACMANUS, Field D, site Kai-Kai, 03843.73?S151840.18?E, 1627 m. Figure 2. Pacmanactis hashimotoi gen. et spec. nov. Preserved specimens. (A) Lateral view of the type material, holotype (NSMT), and paratypes (MNHN on the left and NSMT the two specimens on the centre of the picture). (B) Oral view of holotype and paratype (MNHN), showing the numerous tentacles. (C_/E) Specimen (BEIM) in oral, lateral and aboral view, showing the wider oral disc in comparison with the pedal disc. (F_/G) Specimen NSMT (no type) showing the wider oral disc in comparison with the pedal disc. (H)Detail of the specimen illustrated in G, showing the distinct marginal ridge formed by the sphincter and the short tentacle of the last cycle. Abbreviations: ho, holotype; mr, marginal ridge; od, oral disc; pa, paratype; pd, pedal disc. Scale bars: A_/H, 10 mm. 4 Description.— External anatomy (figs 2, 3): Column smooth, much broader distally than proximally; in preserved specimens diameter up to 12 mm, height up to 12 mm Distal part of the column distinctly marked as a prominent circumferential marginal ridge that contains the distal part of the sphincter (Figure 2B, G, H). Related to directive endocoels distally, a pair of minute ‘tubercle-like’ structures (about 0.25 mm in diameter) (Figure 3D_/F), difficult to observe but visible in the larger studiedspecimens. Pedal disc well developed, adherent, circular, to 10 mm in diameter. Oral disc much wider than column. Tentacles about 100, inner tentacles longer than outer ones, up to 10 mm in preserved specimens (fig. 2B-H), without basal thickening, with a distinct terminal pore. Internal anatomy (figs 3-6): In longitudinal section (fig. 3A), actinopharynx occupying half of the total column length (from pedal disc to oral disc). 5 Figure 3. Pacmanactis hashimotoi gen. et spec. nov. Preserved specimens. (A) Paratype (MNHN) cut longitudinally, showing the wide oral disc, marginal ridge formed by the sphincter, short actinopharynx and filaments on the older mesenteries. (B) Specimen NSMT (no type) cut longitudinally, pharynx is partially protruded to the exterior, but the wider oral disc and the marginal ridge formed by the sphincter are clearly observable. (C) Detail of B, showing the marginal ridge. (D) Detail of the specimen in A, showing the ‘tubercle-like’ structure related to the directive endocoele (arrowed). (E) Detail of D. (F) The same specimens of A, detail of the ‘tubercle-like’ structure related to the opposite directive endocoele showed in D and E. Abbreviations: ap, actinopharynx; co, column; di, pair of directive mesenteries; mf, mesenteric filaments; mr, marginal ridge; ms, mesogloeal sphincter; pd, pedal disc; si, siphonoglyph; te, tentacles. Scale bars: A and C, 5 mm; B, 10 mm; D, 1 mm; E and F, 0.25 mm. Equal number of mesenteries distally and proximally. Mesenteries hexamerously arranged in four cycles, only the first and second cycles perfect and fertile (fig. 4A, B). Two pairs of fertile directives, connected with well-developed siphonoglyphs. Retractor musculature diffuse at actinopharynx level, at lower levels, distalmost mesogloeal arcs more developed than proximal ones. Retractor musculature well developed in the first and second cycles (fig. 4A, B). Third and fourth cycle of mesenteries without filaments. Third cycle with short retractor musculature. Fourth cycle poorly developed, but overlaying gastrodermis thickness. Mesogloea and gastrodermis of the siphonoglyphs slightly wider than the mesogloea and the gastrodermis of the actinopharynx. Parietobasilar musculature not differentiated along the entire mesentery length. Basilar musculature poorly developed (fig. 4C). Gametogenic tissue welll developed in specimens collected in November; gonochoric; developing spermatic vesicles (to 0.23 mm in diameter in preserved specimens). Sphincter muscle mesogloeal, relatively weak, small alveoli well-isolated, slightly hugs epidermal side, occupying all to about three fourth of the mesogloea thickness, (Figure 4D, E). Oral disc (Figure 5ª, B) and tentacles with ectodermal longitudinal musculature (fig. 5C, D). Column wall of similar thickness along entire length. Epidermis 0.04-0.06 mm; mesogloea 0.30-0.40 mm, relatively thick, and gastrodermis 0.06-0.08 mm thick. Cnidom: Spirocysts, basitrichs, holotrichs, microbasic b-mastigophores, and microbasic p-mastigophores. A survey of the cnidae is presented in table 1 and figure 6. 6 Figure 4. Pacmanactis hashimotoi gen. et spec. nov. Holotype. (A) Cross section at actinopharynx level. (B) Detail of A. (C) Longitudinal section of pedal disc. (D) Longitudinal section of margin. (E) Detail of mesogloeal lacunae of the sphincter. Abbreviations: 1, pair of mesenteries of the first cycle; 2, pair of mesenteries of the second cycle; 3, pair of mesenteries of the third cycle; 4, pair of mesenteries of the fourth cycle; ap, actinopharynx; bm, basilar muscle; di, directives; mr, marginal ridge; ms, mesogloeal sphincter; ne, nematocysts; pd, pedal disc; rm, retractor muscle; si, siphonoglyph; te, tentacle. Scale bars: A and B, 1 mm; C and E, 0.2 mm; D, 0.4 mm. 7 Figure 5. Pacmanactis hashimotoi gen. et spec. nov. Holotype. (A and B) Cross section through ectodermal radial oral disc musculature. (C) Cross section of an outer tentacle basally, showing a clear concentration of nematocysts on its aboral side (left side of the photo). (D) Cross section of a tentacle at different level than in C, without concentration of nematocysts, showing mesogloea and ectodermal longitudinal musculature of similar development in oral and aboral sides. (E) Longitudinal section at margin showing the concentration of nematocysts along the oral part of the marginal ridge and basal aboral portion of outer tentacles. (F) Detail of marginal ridge and tentacle; note concentration of nematocysts. Abbreviations: as, aboral side; ep, epidermis; ga, gastrodermis; lm, longitudinal musculature; me, mesogloea; mr, marginal ridge; os, oral side; te, tentacle. Scale bars: A and B, 0.075; C, D and F, 0.2 mm; E, 0.5 mm. 8 Ecological remarks. The trophic behavior of the new species is not known. Maractis rimicarivora, associated with the Mid-Atlantic Ridge hydrothermal vents, can feed on shrimps (Rimicaris exoculata), which particularly abundant on these sites (Van Dover et al., 1997). The actinostolid Marianactis cf. bythios (Van Dover, 2002), wich is very abundant on the recently discovered site Kairei Field (Rodriguez Triple Junction, eastern Indian Ocean), might similarly feed on the shrimps Rimicaris kairei (Van Dover et al., 2001). It is unclear if shrimps are the only prey of the actinostolid anemones. Indeed, within the community of Mariana back-arc basin, where shrimps are not very abundant, the anemone Marianactis bythios was the dominant biomass species inhabiting the periphery of the vents. In comparison to the majority of the Mid-Atlantic Ridge and East Pacific Ridge hydrothermal sites, the Lau, N-Fiji and Manus back-arc basins shelter small sized and less abundant anemones. No anemones were observed at the Manus Basin sites. It is difficult to say if it is the consequence of a declining activity, as it was suggested for the Kai-Kai site, following two observations in 1996 and 1998 (Hashimoto et al., 1999). Pacmanactis hashimotoi has not been identified with certainty outside the areas studied in this paper. However, several ‘whitish’ sea anemones are often recorded by photographic and video devices in many other chemoautotrophic environments, as for example SEPR (South East Pacific Rise, BIOSPEEDO cruise). The detailed study of that material will be the goal of further contributions. Additional studies of the anemones collected by the French cruise BIOLAU and the French-Japanese cruise STARMER in 1989 (Desbruye`res et al. 1994) might give new insights into biogeographic relationships among anemones of the western Pacific back-arc basins, and, in general, in other Pacific vent sites. Acknowledgements The authors thank the Chief scientist Jun Hashimoto of the BIOACCESS’96 and BIOACCESS’98 (Biological Investigation Of A Chemosynthetic Community: Ecological and Systematic Survey) cruises, organized JAMSTEC, and the crew of RV Natsushima and submersible Shinkai 2000, for collecting specimens and making available them for study. Sincere thanks are extended to Shinji Tsuchida (JAMSTEC, Japan), for his improvements to the manuscript. We also thank V. Martin for preparing the map (fig. 1). Partial support was provided by a MCT-CSIC grant (I3P-BPD2001) to Estefanía Rodríguez. Tony Krupa is thanked for reviewing the final English version. The authors are also thankful for comments and suggestions given by Vreni Häussermann and an anonymous referee. References Auzende, J.-M., J. Hashimoto, A. Fiala-Medioni, S. Ohta and E.d. BIOACCESS. – 1997. Etude géologique et biologique in situ de deux zones hydrothermales du bassin de Manus (Papouasie Nouvelle-Guinée). C. R. Acad. Sc. 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