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Terpios Hoshinota, a New Cyanobacteriosponge Threatening Pacific Reefs*

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Terpios Hoshinota, a New Cyanobacteriosponge Threatening Pacific Reefs* SCT. MAR., 57(4): 395-403 SCIENTIA MARINA 1993 RECENT ADVANCES IN ECOLOGY AND SYSTEMATICS OF SPONGES. M.J. URIZ and K. RUTZLER (eds.). Terpios hoshinota, a new cyanobacteriosponge threatening Pacific reefs* KLAUS RUTZLER1 and KATHERINE MUZIK" I Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington. D.C. 205f>O, U.S.A. 2 Muzik. Ink .. 5HO Tremont Street, Boston, Massachusetts 0211H, U.S.A. SUMMARY: The new species Tcrpios hoshinora (Suberitidae, Hadromerida) is described from coral reefs in the western Central Pacific. It is recognized by its extensive grayish to blackish encrustations on coral, distinctive lobed tylostyle spicules, and association with abundant, large, unicellular cyanobacteria of the Apha/locaps raspaigella type. The sponge aggressively competes for space by killing and overgrowing live coral and is responsible for the demise of large reef areas, particularly in pollution-stressed zones near shore. The intercellular zoocyanellae make up half or more of the sponge tissue. Their morphology, as determined by electron microscope observations. is identical to that of symbionts described from two species of an unrelated sponge genus from the Caribbean, Dictyonella. Key Words: Coral Reef. Porifera. competition. symbiosis. cyanobacteria, Pacific. INTRODUCTION Madagascar, 1959). The population density of the starfish varies greatly throughout the Pacific, but re­ For the past two decades or more, coral reefs cently alarming increases have been recorded in some have been increasingly plagued by various pests and areas (CHOAT et at., 1988; GOMEZ, 1988), particular­ other destructive agents. Some of the difficulties they ly in the Ryukyu Islands and elsewhere along the Pa­ are experiencing are due to natural shifts in popula­ cific coast of Japan (YAMAGUCHI, 1987). tion structure that have only recently gained wide­ Sponges have repeatedly been portrayed as im­ spread attention because of the greater abundance of portant space competitors (ROTZLER, 1970, 1971; scientific divers, but man-induced causes have also GLYNN, 1973; VICENTE, 1978, 1990; SUCHANEK et at., had an adverse effect. 1983), but they were not considered a threat to entire The most devastating coral predator in the Pacific reefs until BRYAN (1973) reported unprecedented is the asteroid echinoderm Acanthaster ptanci (L.). spreading of an encrusting Terpios species on the co­ The effect of its population explosions went unno­ ral reefs of Guam. This phenomenon was further ticed until the late 1960s (for a review, see ENDEAN, studied by PLUCER-RoSARIO (1987), who listed the 1973), although outbreaks had been observed almost distribution of the sponge throughout the Northern a decade earlier (Riitzler, unpublished, at Tany Kely, Mariana and Western Caroline Islands, the Philip­ pines, Taiwan, and even American Samoa. In 1985, Muzik (unpublished) confirmed that this sponge oc­ curs on reefs in the Ryukyu Archipelago, first repor­ * Received February 10,1993. Accepted June 2,1993. ted by local newspapers as "black disease." SPONGE THREATENING REEFS 395 128' 'M'~:":.::~~",,~. She"bama *.~ SHIMA {loC::J. 28' Easl 6 Chilla o Yonama Buma Sea *0.*. "• TOKUNO SHIMA -.. ' Japan •• ·C· YORON JIM A '. • • Pati/il' ()('('a 11 126' AGUNI JIMA ";* Ada :06 KUME ." OKINAWA JIM A 26' Ryukyu Archipelago MIYAKO () JIM A ~~.&." • less than 10% live coral •• • YONAGUNI •• 0 " 10% to 50% live coral JIMA •• 0" KOHAMA ~" •••• TARAMA JIMA : •••~" : JIMA * Terpios hoshinota infestation ••"'!e* •• ISHIGAKI ,," ". " SHIMA IRIOMOTE .0.. o 50 100 JIJA .J~ JIM A ·A·· ••• ..I _---'-__'-,_---'-_---'I K i 10m e t e r S 24' 124' 126' FIG, 1. ~ Map of 19R1-19R5 study sites in Japan with location of Tapias hashinota infestations determined in 19R4-19R5, Examination of PLUCER-RoSARIO'S (1987) mate­ MATERIAL AND METHODS rial deposited in the Smithsonian's National Mu­ seum of Natural History and of freshly fixed materi­ Field observations were made in Japan between al from Okinawa revealed that the coral competitor 1981 and 1985, but the sponge described here was not Terpios sp. is an undescribed species. Microscope noted until 1984. Initially, the primary purpose of this preparations also showed an unusually high number work was to inspect the condition of coral reefs in the of large unicellular cyanobacteria present through­ Ryukyu Archipelago (between 123°E, 24°30'N and out the sponge in a type of symbiosis similar to that 130oE, 28°20'N) that had been heavily infested by described from Dictyonella funicularis and D. areno­ starfish (Acanthaster planci) and were located in ar­ sa from the Caribbean Sea (RUTZLER, 1981; both as eas of intensive land development for agriculture, in­ Ulosa). dustry, and tourism (MUZIK, 1985; Fig. 1). During In view of the considerable ecological impact this the survey, more than 300 snorkel and scuba dives sponge is known to have on Pacific coral reefs, our were made to a depth of 40 m. In 1986, sponges were objective in this study was to name and describe the photographed in situ and collected by breaking the species, report on its occurrence and ecology in Japa­ coral substrate. Specimens for systematic study were nese waters, and learn more about the nature of its fixed and preserved in 80 % ethanol. cyanobacterial symbiont. The material used for electron microscopy con- 396 K, RUTZLER and K, MUZIK sisted of l-cm fragments (substrate with sponge crust) Description. - Extremely thin (typically less than fixed in the field in 1.5 % glutaraldehyde buffered in 1 mm thick) encrustations (Fig. 2). In life, the sponge 0.2 M cacodylate with 0.1 M sodium chloride and 0.4 is gray, or dark gray to brownish and black. It is often M sucrose (pH 7.2). The samples were shipped to the lighter in color when growing on the upper surface of National Museum of Natural History in the same me­ corals, darker on the underside. Small (3-mm) oscula dium. After about 10 days, postfixation was carried are usually discernible in the field and are at the cen­ out on 1-2 mm strips of sponge tissue using 2 % os­ ter of radiating, superficial exhalant networks (struc­ mium tetroxide in the aforementioned buffer. Sec­ tures known as astrorhizae from fossil imprints in cal­ tions were stained in saturated (5 %) alcoholic uranyl careous sponge skeletons; Fig. 2c). Pores are located acetate with 0.25 % lead citrate and viewed and pho­ in the meshes of those vein networks. In preserved tographed through a leol 1200 EX electron micro­ specimens, oscula are contracted (closed), and pores scope at 2,000-30,000 x primary magnifications. measure 50-300 [lm. Histological sections show a few Light microscope observations were made on large pores (350 [lm or larger) covered by membranes semithin (1-[lm) sections stained in methylene blue or that are perforated by 10-30 [lm openings. Azure A and on thick sections ground and polished The. sponge grows by lateral propagation, extending to 50-100 [lm sections (ROTZLER, 1978). Spicule size short fine tendrils across crevices to new substrate was estimated in 25 randomly selected tylostyles mea­ (Fig. 2b). The sponge thus advances as a sheet over sured at 100 x magnification for overall length; 10 of platelike·. or massive corals and can make bridges be­ those were also examined at 1,000 x magnification tween branches of corals in species such as Acropora. to determine the maximum diameters of shaft, neck, After sponge encrustation, all polyps die and the re­ and head (knob). maining coral skeleton becomes weak and easy to collect. All spicules of this species are tylostyles. They are RESULTS arranged in criss-cross fashion throughout the choa­ nosome but become organized into radiating bundles Our study of this material led to a review of the near the ectosomal region, where they end in the Suberitidae and a redefinition of the role that Terpios form of brushes at the surface (Fig. 3). The tylostyles species play in this family (see ROTZLER and SMITH, are pin-shaped and are long and slender, only slightly 1993). thickened at midshaft, and have weakly pronounced heads. A typically developed head (tyle) consists of 1. Terpios hoshinota, new species four knobs with axes perpendicular to each other and to the shaft. If the head is subterminal, the blunt end Diagnosis. - Grayish to blackish encrustations on of the shaft forms a fifth knob. The majority of heads, live or dead reef coral in shallow water near shore. however, are strongly reduced and show indications With quadrilobate, often subterminal tylostyle heads. of malformation or erosion (Fig. 4). Measurements Tylostyles, 244.7 [lm x 3.0 [lm (length x maximum are given in Table 1. shaft width); head, 5.6 [lm wide (mean of means, all In some specimens (e.g., USNM 43143), fine sand type specimens). Symbiotic with large (5.9-[lm mean is embedded in the ectosome and is possibly respon­ diameter) intercellular zoocyanellae, which form a sible for the gray color variants. Choanocyte cham­ substantial amount of the cellular tissue in this orga­ bers seem rare or are obscured by the abundance of nism. cyanobacteria; they are oval and measure 20- TABLE 1. - Spicule (tylostyle) dimensions for Terpios hoshinota. Measurements (in ~m) are means ± standard errors. with ranges in parentheses. Specimen. location Total length x Maximum shaft width Neck width Head width Head length Holotype USNM 43144. Japan 251.6±4.8 (180-290) x 3.5±0.1 (3.0-4.0) 2.7±0.1 (2.0-3.0) 6.1 ±0.2 (5.5-7.0) 5.2±0.2 (4.5-6.0) Paratypes USNM 43143. Japan 244.8 5.3 (170-280) x 3.2 0.2 (2.5-4.0) 2.5±0.2 (2.0-3.5) 5.7±0.2 (4.5-7.0) 5.3±0.3 (4.0-7.5) USNM 33316.
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