Species Diversity, 1999, 4, 381-388
First Record of the Order Stauromedusae (Cnidaria, Scyphozoa) from the Tropical Southwestern Atlantic, with a Review of the Distribution of Stauromedusae in the Southern Hemisphere
Priscila A. Grohmann', Mara P. Magalhaes1 and Yayoi M. Hirano2
'Universidade Federal do Rio de Janeiro, Institute de Biologia, Departamento de Zoologia, CCS-Bloco A• Ilha do Funddo, Rio de Janeiro, CEP 21.941-590, Brazil -Marine Biosystems Research Center, Chiba University, Amatsu-Kominato, 299-5502, Japan
(Received 21 April 1999; Accepted 22 July 1999)
Kishinouyea corbini Larson, 1980 is recorded from Santa Cruz, Espirito Santo State, southeastern Brazil. This is the first record of the order Stauromedusae from Brazil, and also from the tropical Southern Hemisphere. Kishinouyea corbini has been known only from two localities in Puerto Rico, and this new record constitutes a great southward extension of the known range of the species. This is also the first report of the species since its original description, so a description of the Brazilian specimens and a comparison with the type material are given. Records of Stauromedusae in the Southern Hemisphere are briefly reviewed. Key Words: Kishinouyea corbini, Stauromedusae, new record, Brazil, range extension, Southern Hemisphere distribution.
Introduction
Stauromedusae are sessile polypoid scyphozoans that generally have a goblet- shaped body and mostly are attached to the substratum by means of an adhesive disc on the base of a stalk-like peduncle of varied length. Uchida (1973) regarded their body as composed of an upper octamerous medusan part and a lower tetramerous scyphistoma polypoid portion. They do not undergo strobilation and do not produce ephyrae. Producing non-swimming planulae (Wietrzykowski 1912; Hanaoka 1934; Otto 1976), they entirely lack a pelagic stage in the life cycle. Stauromedusae feed mainly on small epibenthic crustaceans and gastropods (Bcrrill 1962; Larson 1976, 1980, 1988; Hirano 1986; Larson and Fautin 1989). Stauromedusae are most commonly found in temperate and cold seas, and deep-sea specimens and tropical forms are rarely reported. Only three tropical species have been recorded: Kishinouyea hawaiiensis Edmondson, 1930 from Hawaii; K. corbini Larson, 1980 from Puerto Rico; and Lucemariopsis sp. from the Gulf of Mannar, southern India (Panikkar 1944). The distributions of these three species have not been well documented because none of them has been reported again since their original descriptions. During the course of monitoring an area directly affected by the effluent of a cellulose industrial company ARACRUZ CELULOSE S. A., a stauromedusa was found at Santa Cruz, Espirito Santo State, southeastern Brazil. The stauromedusa was identified as. Kishinouyea corbini Larson, 1980, which had previously been collected only from Joyuda (Capriles and Martinez 1970) and La Parguera (Larson 1980), Puerto Rico. This is the first record of the species away from Puerto Rico, so it is here 382 P. A. Grohmann, M. P. Magalhaes and Y. M. Hirano
Fig. 1. Map showing where Kishinouyea corbini was found in Brazil. redescribed based on Brazilian material. There has been no previous record of the order Stauromedusae from Brazilian waters or from the tropical southwestern Atlantic. Furthermore, this stauromedusa is only the second species found from the whole of South America, whence only Haliclystus auricula (Rathke, 1806) has been known previously from Chile (Kramp 1952; Quezada 1970) and Argentina (Amor 1962). First stauromedusa from tropical SW Atlantic 383
Material and Methods
Santa Cruz is a small village located northwards from Vitoria, the capital of Espirito Santo State (Fig. 1). The climate throughout the entire state is tropical. In the coastal zone it is particularly hot and wet, with a dry season during autumn/ winter (April to September) and a rainy season during spring/summer (October to March). The mean annual air temperature is about 23-24°C. The study area is a marine terrace exposed during low spring tides and covered with lateritic concre tions. Small pools are occupied by Sargassum algae. Because waves are small and highly dissipated due to the shallow water depth, water movement is largely restricted to bottom currents. The specimens were mainly collected from thalli of the alga Sargassum ramifolium Kutzing in shallow subtidal pools at about 0.5 m depth, at low tide. They were taken to the laboratory, where some were carefully relaxed with menthol crystals until the calyxes were fully expanded. Next, they were fixed in 4% formal dehyde solution prepared with sea water. Descriptions were made based on 16 specimens (collected on 20 July 1990, 5 December 1995, 21 March 1996, 14 June 1996, and 30 March 1998). Most of the specimens are housed in the Cnidarian Laboratory Collection of the Universidade Federal do Rio de Janeiro (catalogue codes DZ-IB-UFRJ 1-50 to 1-53). One of the specimens was prepared as histological sections stained with Mallory's triple stain.
Results
The specimens varied in size from 1.2 mm to 12 mm in calyx diameter (exclud ing tentacle clusters). The calyx was shallow and well expanded when relaxed. The margin was divided into four interradial pairs of arms, the perradial notches being two to three times as wide as the interradial ones (Fig. 2). The arms were provided with short, capitate secondary tentacles at the tip, the number of which increased with the size of the calyx, varying from 5-6 in a 1.2-mm diameter specimen up to 21-23 in an 8.9-mm specimen. The outermost tentacles were connected by a pad-like adhesive organ at the base (Fig. 3). All specimens but the smallest one totally lacked primary tentacles. Even in the smallest specimen most of the primary tentacles were already degenerated, and only one reduced primary tentacle remained. The well developed coronal muscle was divided into eight at the arms. Well developed interradial muscles bifurcated in the pyloric region and extended to the tip of the arms. The interradial septa extended from the pylorus almost to the margin of the calyx. The manubrium was short and cruciform with pleated lips. The pylorus contained numerous short gastric cirri, which were readily seen through the transparent oral surface. The gonads comprised several erect, nodular lobes of irregular shape, arranged in eight adradial bands running from the pyloric region almost to the tips of the arms (Fig. 2). Primordia of the gonads were already seen in the smallest specimen, and nodular lobes were discernible in a 1.4-mm diameter specimen. The number of these nodular lobes increased with the size of the specimen: there were 2-3 in the 1.4-mm specimen and 6-7 in the 12-mm one. The white, nematocyst-bearing vesicles were mostly distributed along the calyx 384 P. A. Grohmann, M. P. Magalhaes and Y. M. Hirano
Fig. 2. Oral view of Kishinouyea corbini: st, secondary tentacle; im, interradial muscle; mo, mouth; ve, nematocyst-bearing vesicle; go, gonad lobe. Scale bar — 5mm.
Fig. 3. Aboral view of K. corbini: st, secondary tentacle; ao, adhesive organ; pe, peduncle; im, interradial muscle; ve, nematocyst-bearing vesicle; go, goncid lobe. Scale bar = 5mm. First stauromedusa from tropical SW Atlantic 385
Fig. 4. Side view of K. corbini: st, secondary tentacle; ao, adhesive organ; pe, peduncle; go, gonad lobe. Scale bar = 5mm.
margin and on the nodular lobes of the gonads (Fig. 2), but a few were seen in occasional specimens/radii near the pyloric region of the oral surface. The aboral surface was covered with many evenly scattered and minute warts. The peduncle was short, about 0.3 mm in the 1.4-mm diameter specimen and 1.7 mm in the 12-mm one, terminating in a swollen adhesive disc (Fig. 4). The peduncle was proportionately shorter in larger specimens. It was destitute of interradial muscles and was provided with a cruciform chamber divided into four smaller chambers only at the base. A minute central pit was seen in occasional specimens on the adhesive disc, but no axial canal was present. The colour of living specimens varied, but the predominance of dark green and brown making them accurate mimics of the Sargassum to which they were attached. The gonads were white with brown pigment along the ridges of the nodular lobes. The gastric cirri were translucent reddish-brown tending to pink. Preserved speci mens became pale yellow in formaldehyde solution. Some specimens kept in an aquarium proved to be active, moving their tentacles vigorously and spontaneously in any direction, and also contracting them abruptly at any touch. They were seen to detach themselves and again adhere to Sargassum blades by means of their short peduncle.
Discussion
The material collected at Santa Cruz, ES, Brazil matched the description of Kishinouyea corbini by Larson (1980) and also the type specimens of the species preserved in the National Museum of Natural History, Smithsonian Institution, Washington D.C., but for one feature. According to Larson (1980), the white, nematocyst-bearing vesicles occurred not only near the calyx margin and gonads, 386 P. A. Grohmann, M. P. Magalhaes and Y. M. Hirano
Table 1. Stauromedusae known from the Southern Hemisphere
Species Localities Records
Craterolophus macrocystis New Zealand von Lendenfeld 1884 von Lendenfeld, 1884
Depastromorpha africana South Africa Carlgren 1935 Carlgren, 1935
Haliclystus auricula Chile, Kramp 1952; Quezada 1970 (Rathke, 1806) Argentina Amor 1962
Haliclystus antarcticus South Georgia, Pfeffer 1889; Carlgren 1930 Pfeffer, 1889 Antarctica Carlgren 1930
Haliclystus kerguelensis Kerguelen Island Vanhoffen 1908; Kramp 1957 Vanhoffen, 1908
Kishinouyea corbini Brazil present paper Larson, 1980
Lipkea stephensoni South Africa Carlgren 1933 Carlgren, 1933
Lucernaria australis Antarctica Vanhoffen 1908; Carlgren 1930 Vanhoffen, 1908
Lucemariopsis capensis South Africa Carlgren 1938 Carlgren, 1938
Lucemariopsis vanhoeffeni Antarctica Browne 1910; Carlgren 1930 (Brown, 1910)
Stenoscyphus inabai Australia Mclnnes 1989 (Kishinouye, 1893)
but also near the mouth. In our material, however, they were almost restricted to the calyx margin and to the gonads. But this difference is insufficient grounds for proposing a second species, and so our material is referred to K. corbini. The genus Kishinouyea Mayer, 1910 currently embraces three species, K. nagatensis (Oka, 1897) known from Japan and China, K. hawaiiensis Edmondson, 1930 from Hawaii, and K. corbini Larson, 1980 from the warm western Atlantic. To distinguish K. corbini from its congeners, Larson (1980) enumerated differences such as the nodular, lobe-like gonads and the pad-like adhesive organ at the base of the tentacle clusters, among others. We visited the Bernice P. Bishop Museum, Honolulu, and examined the type specimen of K. hawaiiensis as well as another specimen collected in 1964 at Waikiki. The latter specimen was labelled K. pacifica, which name is apparently a synonym of K. hawaiiensis (Devaney and Eldredge 1977). Both of the Hawaiian specimens have nodular, lobe-like gonads, and, at the base of each tentacle cluster, a pad-like adhesive organ. These characters are neither well illustrated nor described in the original description of K. hawaiiensis by Edmondson (1930), and this has resulted in the furtherance of an erroneous notion thatK corbini is peculiar within the genus, the other two species being more similar each other (Larson 1980). However, K. hawaiiensis is more similar to K. corbini than to K. First stauromedusa from tropical SW Atlantic 387 nagalensis. In this last species the gonads are flat and the bases of the tentacle clusters do not have adhesive organs; in contrast, the outermost tentacles have individual basal swellings. The order Stauromedusae comprises about 45 known species, of which only 10 have been recorded from the Southern Hemisphere. With the present record an eleventh species has been added to the list (Table 1). Four species out of the eleven have not been reported elsewhere than the original locality, and there are only a few records of the others. Stauromedusae seem to be rare and restricted in distribution in the Southern Hemisphere. However, the South African stauromedusa Depastromorpha africana Carlgren, 1935 was recently found also to occur in Australia and New Zealand, whence a few undescribed species were also collected (YMH, unpublished data). These recent discoveries of Stauromedusae from the Southern Hemisphere including the present record of Kishinouyea corbini from Brazil suggest that stauromedusae might be much more common in this hemisphere and that some species might be distributed in a wider area than that from which they are now known.
Acknowledgements
We are indebted to C. Nassar, C. Falcao, and M. C. Maurat for helping us in the collection of the stauromedusae. Thanks are also due to L. A. P. Gonzaga for valuable suggestions, D. Muehe for helping us in mapping the study area, and to C. C. Nogueira for the drawings. We also express our gratitude to R. J. Larson for his encouragement in the preparation of this paper, S. D. Cairns and T. Coffer for the loan of type specimens housed in the National Museum of Natural History, Smithsonian Institution, and the staff of the Bernice P. Bishop Museum for providing the facilities for observing specimens of Kishinouyea hawaiiensis. Special thanks are due to D. R. Calder and M. Yamada for helpful and constructive comments on the manuscript, and to P. F. S.Cornelius for critically reading the manuscript and improving the English.
References
Amor, A. 1962. Sobre Stauromedusae del litoral patagonico Haliclystus auricula (Rathke). Notas del Museo de la Universidad Nacional de La Plata, Zoologia 20: 89-96. Berrill, M. 1962. The biology of three New England stauromedusae with a description of a new species. Canadian Journal of Zoology 40: 1249-1262. Browne, E.T. 1910. Coelenterata V. Medusae. National Antarctic Expedition, 1901-1904. Natural History 5: 1-62, Pis. 1-7. Capriles, V. A. and Martinez, LI. 1970. First report of a Stauromedusae from Puerto Rico. Caribbean Journal of Science 10: 106. Carlgren, O. 1930. Die Lucernariden. Further Zoological Results of the Swedish Antarctic Expedition 1901-1903 2(4): 1-18. Carlgren, O. 1933. Zur Kenntnis der Lucernariiden, Lipkea, Capria und Brochiella. Kungliga Fysiografiska Sallskapets Handlingar N. F. 44(3): 1-19. Carlgren, O. 1935. Uber eine neue siidafrikanische Lucernariide, Depastromorpha africana n. gen., 388 P. A. Grohmann, M. P. Magalhaes and Y. M. Hirano
n. sp. Kungliga Svenska Vetenskapsakademiens Handlingar (3) 15(1): 1-24. Carlgren, O. 1938. Einc neue sudafrikanische Luccrnariidae, Lucemariopsis capensis. Kungliga Fysiografiska Sallskapets i Lund Forhandlingar 8(11): 1-6. Devaney, D. M. and Eldredge, L. G. 1977. Class Scyphozoa. Pp. 108-118. In: Devaney, D. M. and Eldrcdge, L. G. (Eds.) Reefand Shore Fauna ofHawaii. Section 1: Protozoa through Ctenophora. Bernice P. Bishop Museum Special Publication 64(1), Honolulu, 278pp. Edmondson, C. H. 1930. New Hawaiian medusae. Bernice P. Bishop Museum Occasional Papers 9(6): 1-16. Hanaoka, K. 1.1934. Notes on the early development of a stalked medusa. Proceedings of the Imperial Academy of Japan 10: 117-120. Hirano, Y.M.I986. Studies on Stauromedusae (Coelenterata, Scyphozoa) in Hokkaido - distribution and life history (Abstract). Benthos Research 30: 10-13. [In Japanese] Kramp, R. 1952. Reports on the Lund University Chile Expedition 1948-49. 2. Medusae collected by the Lund University Chile Expedition 1948-49. Kungliga Fysiografiska Sallskapets Handlingar N. F. 62(7): 1-19. Kramp, P. 1957. Medusae. B. A. N. Z. Antarctic Research Expedition, 1929-31, Ser. B, 6: 151-164. Larson, R.J. 1976. Marine Flora and Fauna of the Northeastern United States. Cnidaria: Scyphozoa. NOAA Techical Report NMFS Circular 397: 1-18. Larson, R. J. 1980. A new stauromedusa, Kishinouyea corbini (Scyphozoa, Stauromedusae) from the tropical western Atlantic. Bulletin of Marine Science 30(1): 102-107. Larson, R.J. 1988. Kyopoda lamberti gen. nov., sp. nov., an atypical stauromedusa (Scyphozoa, Cnidaria) from the eastern Pacific, representing a new family. Canadian Journal of Zoology 66:2301-2303. Larson, R. J. and Fautin, D. G. 1989. Stauromedusae of the genus Manama (= Thaumatoscyphus) (Cnidaria, Scyphozoa) in the northeast Pacific, including descriptions of new species Manama gwilliami and Manania handi. Canadian Journal of Zoology 67: 1543-1549. Lendenfeld, R. von 1884. The Scyphomedusae of the Southern Hemisphere. Proceedings of the Linnean Society of New South Wales 9: 155-169. Mclnnes D. E. 1989. A stalked jellyfish (Stauromedusae), found at Black Rock, Port Phillip Bay. A first recording in Australia. Victorian Naturalist 106(3): 86-92. Otto, J.J. 1976. Early develoment and planula movement in Haliclystus (Scyphozoa, Stauro medusae). Pp. 319-329. In: Mackie, G. O. (Ed.) Coelenterate Ecology and Behaviour. Plenum Press, New York, 744pp. Panikkar, N. K. 1944. Occurence of a stauromedusa on the Indian coast. Current Science 13(9): 238-239. Pfeffer, G. 1889. Zur Fauna von Sud-Georgien. Mitteilungen aus dem Naturhistorischem Museum zu Hamburg 6: 16. Quezada, A.E.I970. Haliclystus auricula (Rathke 1806) (Coelenterata, Scyphozoa, Stauro medusae) en el golfo dc Arauco (Chile). Boletin de la Sociedad Biologica de Conception 42: 75-80. Uchida, T. 1973. The systematic position of the Stauromedusae. Publications of the Seto Marine Biological Laboratory 20: 133-139. Vanhoffen, E. 1908. Die Lucernariden und Scyphomedusen der Deutschen Siidpolar-Expedition 1901-1903. Deutschen Siidpolar-Expedition 10: 25-49, Pis 2, 3. Wietrzykowski, W. 1912. Recherches sur le developpement des Lucernaires. Archives de Zoologie Experimental et Generate (5) 10: 1-95.