C. Aprica – C. Langae (Porifera, Hadromerida, Clionaidae)

Taxonomy of the Caribbean excavating sponge species complex Cliona caribbaea – C. aprica – C. langae (Porifera, Hadromerida, Clionaidae)

SVEN ZEA1 AND ERNESTO WEIL2

1Departamento de Biologı´a y Centro de Estudios en Ciencias del Mar – CECIMAR, Universidad Nacional de Colombia, INVEMAR, Cerro Punta de Betı´n, A.A. 10-16, Santa Marta, Colombia, [email protected] 2Department of Marine Sciences, University of Puerto Rico, Islas Magueyez Marine Laboratory, P.O. Box 908, Lajas, Puerto Rico 00667, [email protected]

ABSTRACT.—In the Caribbean Sea, brown to brown-black sponges that both excavate and encrust calcar- eous substratum are variably and confusedly reported as Cliona caribbaea, C. aprica and/or C. langae (Family Clionaidae, Order Hadromerida). They extend sideward undermining and displacing live coral tissue. To resolve the taxonomy of the species, detailed observations and sampling were carried out in Colombia, Venezuela, Curac¸ao, Belize, Jamaica and Puerto Rico. Differences in external morphology and color, and subtle, but consistent differences in spicule morphology and size, revealed the existence of three distinct species, Cliona aprica Pang, 1973, Cliona caribbaea Carter, 1882 (junior synonym C. langae Pang, 1973), and Cliona tenuis sp. nov. C. aprica consists of brown-black, closely spaced papillae that may fuse to form an incomplete thin crust. C. caribbaea is amber brown, often fully encrusting, with thicker (up to 2 mm) tissue and conspicuous oscules, often riddled with zoanthids. C. tenuis covers the entire substratum with a thin, transparent veneer of brownish tissue; oscules are small and inconspicuous. Spicule morphology and size show geographical variation but remain distinctive for each species within a given locality. Most of the recent substratum monopolization and coral tissue death from species of this complex in many Caribbean fore reefs is attributable to C. tenuis.

INTRODUCTION of cm year−1) and extensive death of coral tissue (Ru¨ tzler 1975, 2002b; Acker and Among the sponges that are able to ex- Risk 1985; Scho¨nberg and Wilkinson 2001; cavate tunnels and galleries into carbonate Lo´pez-Victoria et al. in press). As a result of materials, there are some that also encrust, local population increase of some of the partly or entirely, the surface of the exca- species, the marine scientific community vated substratum. In the Caribbean Sea, became interested in dark brown clionaids. those with a dark brown to brown-black The population change seems to have color have been variably reported as Cliona started around early 1980’s, apparently as a viridis (Schmidt 1862), C. caribbaea Carter result of increased stress and massive mor- 1882, C. aprica Pang 1973a, and/or C. langae talities in corals associated to bleaching, Pang 1973a (Family Clionaidae, Order disease and high temperature (Corte´s et al. Hadromerida, Class Demospongiae, cf. 1984; Ru¨ tzler 2002b). They have since mo- Ru¨ tzler 2002a). These sponges dig a shal- nopolized ample reef space in some locali- low valley in the substratum, which may ties and as a result additional tissue loss has extend over several square meters. But occurred in colonies of the most common their tissue penetrates only about 1.5-2 cm reef-building corals (Williams et al. 1999; below the surface, excavating chambers Ru¨ tzler 2002b). These observations prompted and galleries which are completely filled us to study these sponges in some areas of with dark yellow tissue. As these sponges the Caribbean Sea and led us to new taxo- encounter live coral tissue, their lateral ex- nomical and morphological definitions. tension continues on with the aid of exca- Considerable taxonomic confusion has vating pioneering tissue threads, which occurred with the species involved, which undermine the polyps skeletal support, promoted the use of the term “complex” to resulting in relatively fast (in the order signal suspected genetic heterogeneity. On 348 TAXONOMY OF CARIBBEAN EXCAVATING SPONGE 349 the substratum these excavating sponges pose of this paper is to describe and illus- may appear either as isolated to partially trate these three species of Cliona, and fused fields of papillae, or as a continuous provide information on their geographical encrusting sheet, thin when the sponge variability. grows actively, and thick when it stops its sideward growth; papillae may also occur at the edges of some encrusting specimens MATERIALS AND METHODS (see Lo´pez-Victoria et al. in press). Geo- graphical variation in the predominant Extensive observations and sampling morphology, and in spicule morphology were carried out in several areas of the and size, made it difficult to define species. south (continental coast of Colombia) and The studied species were grouped within southwestern (San Andre´s and Old Provi- the larger “Cliona viridis complex” that dence Archipelago, Colombia) Caribbean comprises Atlantic, Mediterranean and Sea. Visits to other areas (Belize, Jamaica, Indo-Pacific species (Scho¨nberg 2002 and Puerto Rico and Venezuela) yielded further references therein). For the Caribbean, material for comparisons (Fig. 1). Material Carter (1882) originally described Cliona and observations from Curac¸ao were pro- caribbaea from St. Vincent, Lesser Antilles. vided by M. Lo´pez-Victoria. Later, Topsent (1900) put it into synonymy Fragments of sponges encrusting the with Mediterranean Cliona viridis (Schmidt substratum were obtained with hammer 1862); this decision was followed in other and chisel or a corer, fixed in 96% ethanol taxonomic studies in the Caribbean (e.g., or in 10% formalin in seawater buffered Hechtel 1965). However, Ru¨ tzler (1974) re- with methenamine (20 g l−1), and preserved described Cliona caribbaea as a valid Car- in 70% ethanol after 2-3 days. Small frag- ibbean species. Contemporary to the latter ments of sponge tissue with substratum author, Pang (1973a) described two new were digested in commercial bleach to ob- species, Cliona aprica and C. langae, but mis- tain clean siliceous spicules suspensions; or takenly described material of a different they were fully decalcified in 5% nitric acid species under the name Cliona caribbaea. solution. Spicule suspensions or decalcified From then on, most sponge and coral reef tissue were boiled in fuming nitric acid. workers used Pang’s monograph and iden- Permanent spicule slides were prepared tified the brown encrusting reef clionaids for microscopic examination according to as either C. aprica or C. langae (e.g. Ru¨ tzler Ru¨ tzler (1974). Spicules of several speci- 1975; Humann 1992) and largely ignored mens, from each sampled area, (see Table C. caribbaea (but see Acker and Risk 1985) 1) were measured under a Leitz Wetzlar or followed Pang’s mistake (e.g. Hofman compound microscope. For megascleres and Kielman 1992). Recently, Ru¨ tzler (tylostyles) we measured, at 125×, the fol- (2002b) hypothesized that C. aprica, C. car- lowing: total length, maximum width of ibbaea and Cliona langae represent a single, shaft, and length and width of the head of highly variable species, whose name 25 spicules per specimen. Total length, should be C. caribbaea. This idea was pro- width of shaft, largest width of the spire, posed in spite that two to three distinct number of spiral turns, and length of the forms had previously been distinguished longest spire (equivalent to largest wave- by other workers (Pang 1973a; Acker and length, if the spiraster is seen as a projected Risk 1985; Zea 2001). In a recent visit to sinusoidal wave) of 10-15 microscleres (he- Jamaica as part of this study, three morpho- lical spirasters) per specimen, were mea- types were found sympatrically at the fore sured at 1250× with immersion oil. reef of Discovery Bay; thus, allowed us de- Internal morphology of sponges was ex- tailed comparisons. After re-examination of amined microscopically using sections of all Caribbean samples collected by the au- sponge-substratum fragments that were: thors and some museum material, the three cut and trimmed with a low-speed dia- morphotypes were recognized as good spe- mond circular saw (Isomet™, Buehler, Chi- cies, subtly, but clearly different. The pur- cago); embedded in low viscosity Spurr 350 SVEN ZEA AND ERNESTO WEIL

FIG. 1. Map of the Caribbean Sea showing the distribution of the three species in the sampled areas. resin (ERL 4206, Electron Microscopy Sci- INVEMAR – Museo Nacional de Historia ences, Fort Washington, Philadelphia); cut Natural Marina de Colombia Porifera col- and glued onto microscope slides; cut lection at Santa Marta (INV-POR), and at again, ground to ca. 20-50 ␮m in thickness the Instituto de Ciencias Naturales, Museo with a graded series of diamond coated de Historia Natural, Universidad Nacional abrasive paper; and polished with commer- de Colombia at Bogota´ [ICN-MHN(Po)]. cial aluminum oxide metal polisher, in a We also analyzed spicule slides, tissue frag- petrography grinder/polisher (Minimet ments, digital photographs and/or draw- 1000, Buehler) (after Ru¨ tzler 1974; Willenz ings from Washington National Museum of and Pomponi 1996). Staining was carried Natural History (USNM), London British out for 5-15 min with basic (or acid) fucsin Museum of Natural History (BMNH), Yale and crystal violet, either during the dehy- Peabody Museum (YPM), and City of drating process previous to embedding, or Liverpool Museum (LIVCM). Color codes directly on the polished sections (the latter are those of the American Museum of on a warm slide plate). Natural History Naturalist’s Color Guide Underwater photographs of sponges (Smithe 1975) and indicated as NCG. Num- were taken with a Nikonos V 35 mm film bers of studied specimens were: Cliona camera assembled with a SB-105 strobe and aprica, 54; C. caribbaea, 28; C. tenuis, 41. Col- close up and macro-ring attachments. Spic- lection number is boldfaced for those speci- ules and sections were drawn using a cam- mens whose spicules were measured era lucida. Digital scanning electronic mi- (Table 1). crographs (SEM) of spicules from some specimens were kindly made by K. Ru¨ tzler RESULTS and M. Nestlerode (Smithsonian Institu- Common characteristics of the studied tion, Washington, DC). species complex Unless noted, samples were collected by S. Zea and deposited at the Instituto Excavating. Fields of papillae to com- de Investigaciones Marinas y Costeras – pletely encrusting. Level of substratum TAXONOMY OF CARIBBEAN EXCAVATING SPONGE 351 usually slightly lower than surroundings. Pl. 1 (A, C, E), Pl. 2 (A, D, G, J). Fig. 2 (A), Fig. Surface brown to brown-black. Oscules 3 (A, D, G, J), Figs. 4-6 small, up to 2.3 mm in diameter (Pl. 1). Cliona aprica Pang 1973a: 42, forma aprica,p. When thick enough to allow judgment, 43, figs. 12, 21 (Jamaica, shallow form, 0-5 m, consistency leathery, velvety to the touch. holotype YPM 8772), forma profunda, p. 45, fig. Sponge penetrates and excavates substra- 13 (deep form, 12-34 m, paratype YPM 8723) (other paratypes at BMNH and State University tum up to 2 cm beneath surface. Ectosome of New York at Stony Brooks-University of West over excavated troughs a palisade of verti- Indies); Pang 1973b (Jamaica, ecology); Tunnic- cally oriented tylostyle spicule brushes, of- liffe 1979: 309 (Jamaica, role in coral fracture); ten separated by incurrent canals; top of D´ıaz et al. 1995 (San Andre´s, in part, lagoonal shallow substratum rims with paratangen- and leeward records; windward records are for tially placed spicules (Fig. 2). Choanosome Cliona tenuis); Lehnert and van Soest 1998: 79 fleshy, dark yellow, filling entirely coral- (Jamaica, referring to the type material); Lo´pez- calicular spaces and excavating chambers; Victoria et al. in press (Colombia, biology). sub-superficial color frequently olive green. ?Cliona aprica; Alcolado, 1976: 6 (Cuba); 1979: When growing in flat or cylindrical coral 112, table 2; 1989: 6, table 1; 1990: 352; 1999: 121 branches, excavating tissue filaments (1-2 (Cuba, distribution); MacGeachy 1977: 479 (Bar- mm in diameter) may cross entire expanse bados, factors controlling erosion); Vacelet 1981: of coral skeleton. When growing into live 717 (Guadeloupe, ultrastructure of zooxanthellae); Buznego and Alcodalo 1987; 7 (Cuba, ero- coral tissue, pioneer filaments and cham- sion in corals). bers undermine below coral polyps over Non Cliona aprica;Ru¨ tzler 1975: 205 (Belize, several cm (see also Lo´pez-Victoria et al. in bioerosion rates); Pulitzer-Finali 1986: 95 (Puerto press). Threads of fusiform contractile cells Rico); Vicente 1990a: 200 (Puerto Rico, zooxan- (fide Ru¨ tzler 1974) common below spicule thellate symbionts); 1990b: 439, fig. 4 (Puerto brushes and lining coral skeleton near top Rico, overgrowth by other organisms) [All are of substratum rims. Choanosomal tissue Cliona tenuis]. with loosely arranged tylostyles. Rows of Cliona caribbaea; Hofman and Kielman 1992: tylostyles occur near and in parallel to 206, fig. 9 (Colombia, in part, only specimen walls of excavated troughs, accompanied INV-POR 0406; specimens INV-POR 0397 and 0411 are Cliona flavifodina Ru¨ tzler 1974); Ru¨ tzler by connective tissue threads. 2002b: 64, fig. 4.1 (Belize, in part, only some pap- Choanosomal canals often lined by spi- illose specimens). raster spicules. Superficial tissue packed Non Cliona caribbaea Carter 1882 (a valid spe- with intracellular zooxanthellae, 9.2-11.5 cies). ␮m in diameter, sparser further inside but Cliona aprica – C. langae – C. caribbaea species occur throughout the choanosome, includ- complex; Valderrama 2001: 31 (morphotype 1, ing excavating pioneering filaments. All in- Gulf of Uraba´). ternal surfaces of substratum with typical Cliona sp. 1; Zea 2001 (SW Caribbean atolls, concave marks of removed carbonate chips, distribution). even on top of rims. Megascleres: tylo- Non Cliona sp. 1; Zea 1993: 87 (Santa Marta, distribution, = Cliona flavifodina Ru¨ tzler, 1974). styles with rounded to slightly elongated heads (Pl. 2; Fig. 3). Microscleres: slender, thin spirasters with relatively small spines Studied material.—Jamaica. Discovery lined in the convex side. Size of spicules Bay, Dairy Bull, 8 m: ICN-MHN(Po) 177, varies with locality, tylostyles generally INV-POR 609, POR 610; Fore reef: 9-30 m, larger and more robust and spirasters INV-POR 611, 612, 613, 614. Curaçao. (all thicker at continental coast of Colombia by M. Lo´pez-Victoria) Playa Kalki: 4 m, Fig. (see Table 1, Figs. 4-6). P1 live 4/CICN-MHN(Po) 181; Santa Marta Baai: 5-6 m, INV-POR 623; Blauwbaai: 10.5 Species descriptions m, INV.POR 624, 625. Venezuela. Los Order Hadromerida Topsent, 1894 Roques Archipelago, Dos Mosquises: 16 m, Family Clionaidae D’Orbigny, 1851 INV-POR 619. Continental coast of Colom- Genus Cliona Grant, 1826 bia. Santa Marta, Bah´ıa de Nenguange: 1-3 m, Cliona aprica Pang, 1973 ICN-MHN(Po) 179, INV-POR 618, Hofman 352 SVEN ZEA AND ERNESTO WEIL ) 3 Belize 4-9 (6.7 ± 1.7) 2-5 (3.5 ± 0.3) (mean ± 1 standard 1.0-3.0 (2.1 ± 0.2) 1.2-2.0 0.5-1.0 (0.71 ± 0.18) 0.8-1.5 (1.08 ± 0.05) 1.0-2.0 2.0-5.0 (3.3 ± 0.2) 0.5-1.0 (0.8 ± 0.3) 0.7-1.8 (1.03 ± 0.05) 10-17.6 (13.8 ± 0.6) 8.5-15.5 (12.0 ± 0.8) 8.1-16.6 (12.9 ± 0.3) 5.2-13.3 (9.0 ± 0.6) 280-413 (351±26 9.5-19.0 (12.9 ± 1.3) Profuse, in bouquets 22.0-47.0 (37.3 ± 4.8) Sparse, mostly unbranched and 10-15 spirasters). In the ) 17.0-33.0 (24.6 ± 2.2) ) 8.5-17.6 (12.2 ± 0.9) ) 261-399 (332 ± 21) 1.6) 7.6-15.7 (12.0 ± 0.6) 3-7 (4.3 ± 1.3) Venezuela 1.5-2.0 2.7-5.0 (3.9 ± 0.7) 0.7-1.0 (0.9 ± 0.1) 1.0-2.7 (1.3 ± 0.4) 3.8-5.7 (5.0 ± 0.5) 4.3-13.3 (8.2 ± 1.3) 204-333 (332±25 for those individuals measured is marked in bold ) ) 1 513 1.0 2-8 (4.3 ± 0.7) 5-10 (7.6 ± 1.4) Colombia** 1.5-3 (2.3 ± 0.5) 3.8-19 (12.0 ± 2.5) sp. nov. at each geographic area. Data are min.-max. 0.5-1.5 (0.9 ± 0.3) 0.8-1.1 (0.9 ± 0.1) 1.0-2.5 2.3-8.1 (4.3 ± 0.7) 0.5-1.7 (1.1 ± 0.3) 0.8-1.5 (0.9 ± 0.02) 10-11.5 (10.6 ± 0.6) Area 7.1-15.2 (12.0 ± 2.2) 313-418 (379±31 8.3-19.2 (11.9 ± 0.5) 10.5-15.0 (12. ± 1.8) 9.0-19.5 (15.5 ± 2.2) 3.8-10.5 (8.6 ± 270-427 (357±9 25.5-43.5 (36.3 ± 6.0) 10.5-17.6 (14.3 ± 1.7) 10.0-18.1 (15.1 ± 1.7) 14.9-38.5 (26.0 ± 3.2) 20.0-33.5 (26.1 ± 3.5 10.4-19.0 (16.0 ± 0.4) 8.5-12.8 (10.5 ± 1.0 Profuse, in bouquets Profuse, in bouquets Sparse, mostly unbranched C. tenuis specimens measured (which came from 25 tylostyles and n Rico Puerto ) ) ) ) ) 0.7) Jamaica 2-7 (4.5 ± 0.5) 2-10 (5.6 ± 0.7) Cliona aprica, C. caribbaea 9-14.5 (11.7 ± 1.4) deviations refer to that set of data only. Collection number 0.5-2.0 1.5-3.5 (2.6 ± 0.3) 0.5-1.5 (1.02 ± 0.08) 0.7-2.0 2.0-5.5 (3.4 ± 0.8) 0.5-1.0 (0.7 ± 0.04) 0.7-1.4 (0.92 ± 0.08) 4.7-14.3 (10.2 ± 1.2) 275-465 (370±33 237-394 (324±15 4.7-10.0 (7.5 ± 1.7) Profuse, in bouquets from mean sizes of each of Sparse, mostly unbranched ) ) ) ) s ´ 85 94 1-9 (4.1 ± 1.4) 2-6 (3.5 ± 0.5) San Andre Archipelago* 1.0-2.0 0.3-1.4 (0.73 ± 0.25) 0.3-1.1 (0.59 ± 0.14) 0.6-2.0 0.4-1.0 (0.7 ± 0.1) 8.5-26.0 (12.9 ± 3.6) 7.5-21.0 (13.2 ± 2.6) 7.1-17.1 (12.1 ± 2.0) 7.1-17.1 (13.0 ± 1.3) 7.1-15.2 (11.3 ± 1.7) 8.1-15.7 (12.9 ± 4.7-13.3 (8.4 ± 1.7) 271-418 (340±26 8.6-21.8 (12.5 ± 1.3) 7.1-15.7 (11.8 ± 1.0) 8.1-15.2 (10.8 ± 0.8) 6.6-15.7 (12.3 ± 0.9) 8.1-14.3 (11.8 ± 0.4 232-375 (301±21 4.7-14.2 (8.5 ± 0.6) 14.9-46.0 (26.7 ± 5.3) 22.0-45.5 (33.7 ± 4.7 12.6-34.0 (21.5 ± 2.4) 16.0-33.0 (24.5 ± 1.7 1. Measurements and spicule characteristics of spire spire Length of longest Spine height Number of turns Spine branching Profuse, in bouquets Spire max. diameter 2.0-5.0 (2.8 ± 0.6 Shaft width Length Head length/width 0.7-1.7 (1.08 ± 0.17) Head length Head width Shaft width Length Length of longest Spine height Number of turns Spine branching Profuse, in bouquets Spire max. diameter 2.3-7.0 (4.5 ± 0.6 Shaft width Length Head length/width 0.5-1.9 (0.96 ± 0.06) Head length Head width Length Shaft width ABLE T Spirasters Tylostyles Spirasters Tylostyles Cliona caribbaea Specimens studied deviation). Mean and standard deviation calculated case of single specimen samples, means and standard in the material studied section for each species. Species/spicule Cliona aprica Specimens studied TAXONOMY OF CARIBBEAN EXCAVATING SPONGE 353 ) 3 1-5 (2.7 ± 0.3) 1.0-1.5 3.0-6.0 (4.3 ± 0.3) 0.8-1.6 (1.06 ± 0.07) 8.1-14.3 (11.4 ± 0.3) 7.6-14.3 (10.9 ± 0.4) 4.7-12.3 (7.5 ± 0.9) 214-380 (308±15 Profuse, in bouquets 14.0-25.5 (16.4 ± 2.0) 0.40-1.25 (0.70 ± 0.14) 18.5-39.0 (24.8 ± 1.3) Venezuela Belize ) ) ) ± 1.6) 23.8 ± 2.9) 1.2-1.7 Colombia** 1.0-7.0 (3.7 ± 0.7) 2.0-8.0 (4.2 ± 0.9) 0.3-1.3 (0.9 ± 0.2) 4.7-14.3 (9.4 ± 1.2) ) 219-370 (300±20 Area ± 1.0) 7.4-43.7 (13.7 ± 1.1) Rico Puerto 0.7-1.5 1-6 (4.3 ± 0.4) 2.0-5.0 (2.8 ± 0.2) 0.5-1.1 (0.7 ± 0.2) 204-275 (246±3 7.6-13.3 (9.8 ± 0.6) 7.1-16.6 (12.4 ± 1.4 0.8-1.6 (1.06 ± 0.06) 0.8-1.5 (1.11 ± 0.15 Profuse, in bouquets Profuse, in bouquets ) 7.1-14.3 (10.6 ± 1.3) 9.0-18.5 (12.9 ) 1.5) 20.5-27.0 (24.4 ± 0.1) 12.0-37.5 ( 0.7-1.0 Jamaica 1-4 (2.7 ± 0.2) 3.0-8.0 (4.8 ± 0.5) 0.5-0.7 (1.0 ± 0.1) 3.8-8.1 (5.6 ± 0.2) 5.2-12.8 (7.7 ± 0.5) ) 219-299 (258±2 0.7) 10.5-25.0 (16.9 ± 2.4) 9.5-14.0 (11.7 s ´ 6226 1.2-2.0 San Andre Archipelago* 1-5 (3.6 ± 0.5) 2.3-6.9 (4.1 ± 0.7) 0.5-1.1 (0.7 ± 0.1) 3.3-9.5 (6.3 ± 1.0) 7.1-13.8 (9.9 ± 0.1) 7.1-10.9 (9.3 ± 0.6 5.7-13.3 (9.7 ± 0.9) 7.1-11.4 (9.2 ± 0.1) 199-321 (268±21 0.7-1.8 (1.00 ± 0.09) 0.8-1.8 (1.02 ± 0.07) 11.0-30.0 (22.7 ± 2.3) 17.0-39.0 (24.3 ± Profuse, in bouquets Profuse, in bouquets sp. nov. 1. Continued. Length of longest spire 9.7-20.7 (12.5 ± Spine height Number of turns Spine branching Spire max. diameter Shaft width Length Head length/width Head length Head width Shaft width Length ABLE T *SW Caribbean, but belongs**Continental to coast Colombia Spirasters Tylostyles Cliona tenuis Specimens studied Species/spicule PLATE 1. Underwater close-up photographs of the studied sponges. Cliona aprica (A, C-right, E), C. caribbaea (B, D, F), C. tenuis (C-left, G, H). (A) Quitasuenõ Bank, on Montastraea annularis, lagoon, 3 m. (B) San Andre´s Island, leeward terrace, 13 m. (C) Discovery Bay (Jamaica) shallow fore-reef, 4-5 m. (D) Belize, barrier fore reef, 27 m. (E) Islas del Rosario, on a dead coral branch, lagoon, 4 m. (F) Islas del Rosario, 18-21 m. (G) Quitasuenõ Bank (San Andre´s Archipelago, Colombia), fore reef terrace, in coral Diploria strigosa, 2 m. (H) Islas del Rosario (continental Colombia), fore reef, in coral Diploria labyrinthiformis, 6 m. Width of field aprox. 16.4 cm. TAXONOMY OF CARIBBEAN EXCAVATING SPONGE 355

593, 595, 597, 598, M. Lo´pez-Victoria, 627, 628; Top Blowing Rocks: 1 m, INV-POR 599; Bajo Bonito: 12 m, M. Lo´pez-Victoria, INV-POR 626. Courtown (=Bol´ıvar) Cays: 3-8 m, INV-POR 600, ICN-MHN(Po) 175. Old Providence Island, Filo Point: 0.8-2 m, INV-POR 601. Serrana Bank: 1.5-20 m, ICN- MHN(Po) 176, INV-POR 602, 603, 604, 605, 606, 607. Quitasuen˜o Bank: 15 m, INV-POR 608. Belize. Carrie Bow Cay area, Carrie Bow Cay: 0.5-21 m, ICN-MHN (Po) 180, INV-POR 620, 622; North of South Water Cay: 0.5, INV-POR 621. Diagnosis.—Fields of papillae, fused partly to almost completely in a thin (up to 1 mm) encrusting sheet. Size up to about 50 cm in diameter. Dark brown to brown black. Oscules up to 1.9 mm in diameter, sometimes with grayish rim. Tylostyles with rounded heads, 232-427 ␮m long by 3.8-19.0 ␮m wide. Spirasters wide turning, 12.6-38.5 ␮m long, 0.4-1.7 ␮m thick, with usually 2-4, rarely up to 8 turns; maximum width of spires 2.0-8.0 ␮m; spines in branching bouquets, up to 2.5 ␮m tall. Morphology.—Groups of inhalant and ex- halant papillae, rather small, 0.7-3.7 mm in diameter, dark brown to black (NCG 19- Dusky brown, 20 and 129-Dark grayish brown), on shallow (up to about 1 cm deep) substratum valleys. Papillae usually fuse extensively as sponge grows sideward, covering most of substratum, but leaving scattered uncovered islands of carbonate FIG. 2. Camera lucida drawings of sponge-coral fouled by algae and other organisms. When substratum sections, ground and polished, of encrusting specimens. (A) Cliona aprica on Siderastrea siderea; growing over and inside coral branches or (B) C. caribbaea on Montastraea cavernosa; (C) C. tenuis rubble, papillary fusion is poor; fully re- sp. nov. on Diploria strigosa. laxed papillae protrude 1-2 mm above substratum. When growing on massive corals and M. Kielman, 406. Rosario Islands, Pa- or limestone pavement (especially at San jarales, San Mart´ın: 1-3.6 m, ICN-MHN(Po) Andre´s Archipelago and Jamaica), fusion 178,M.Lo´pez-Victoria, INV-POR 630; Isla frequently more extensive. Size up to 50 cm Grande, Cocoliso, on sea-grasses: 0.5 m, M. to1minthelongest diameter. Oscules Lo´pez-Victoria, INV-POR 616; Bajo del Me- 0.9-1.9 mm in diameter, inconspicuous or dio: 4 m, INV-POR 615. San Bernardo Is- with whitish or grayish collar (NCG 80- lands, Mu´ cura: 0.5 m, INV-POR 617.NW Glaucous, 81-Pearl Gray). Only few speci- Gulf of Uraba´, Cabo Pinololo: 6 m, INV- mens colonized by light yellow zoanthids. POR 577. San Andre´s and Old Providence Depth of excavation 4-19 mm beneath the Archipelago (Colombia). San Andre´s Is- surface. Fully excavated areas below papil- land, Half a Reef: 0.5-5 m, ICN-MHN(Po) lae or oscules up to 3.3 mm wide and 6.7 174, INV-POR 594,M.Lo´pez-Victoria, 596; mm deep. Elevated rims of substratum not Wildlife, 4.5-13 m: INV-POR 585, 586, 587, fouled by organisms covered by a thin tis- 588, 589, 590, 591, 592, M. Lo´pez-Victoria, sue layer. Solid areas excavated by tunnels 356 SVEN ZEA AND ERNESTO WEIL

PLATE 2. SEM images of spicules. Cliona aprica (A, D, G, J); C. caribbaea (B, E, H, K); C. tenuis sp. nov. (C, F, I, L). Scale bars for A-C 100 ␮m; for D-L, 2 ␮m. and circular chambers 67 ␮m to 3.3 mm in scleres: thin spirasters with wide spires, diameter. Tissue traversed by canals 50-760 profusely spined; spines branched, forming ␮m in diameter. bouquets; spiraster tips with rather elabo- Spicules.—Tylostyles, usually with round rate spine bouquets. Spirasters usually with heads, generally slightly vertically com- 2-4 turns, rarely up to 8 turns; the widest pressed (length/width < 1); shafts robust or spire usually located centrally; lateral slender, usually slightly curved. Measure- spires often smaller and asymmetrical. ments (Table 1, range of means): length Measurements (Table 1, range of means): 301-357 ␮m, shaft width 5.0-12.0 ␮m, head length 21.5-26.1 ␮m, shaft width 0.7-1.1 width 8.6-15.5 ␮m, head length 10.5-16.0 ␮m; spire maximum diameter 3.3-4.5 ␮m; ␮m. Heads at San Andre´s Archipelago, Ja- number of turns 3.5-4.5; longest spire maica and continental coast of Colombia length 11.7-12.9 ␮m. Spine height (total predominantly compressed to rounded min.-max.) 0.6-2.5 ␮m. (length/width 0.90-0.96), at Belize rounded Distribution.—Jamaica, Curac¸ao, Venezu- to slightly elongated (1.03), at Venezuela ela (Los Roques Archipelago and Morro- quite elongated (1.29) (Fig. 4A). Micro- coy), continental coast of Colombia (Santa TAXONOMY OF CARIBBEAN EXCAVATING SPONGE 357

FIG. 3. Comparative view of camera lucida drawings of spicules of the three species at San Andre´s Island (A-C), Jamaica (D-E), continental coast of Colombia (G-I) and Belize (J-L). Cliona aprica (A, D, G, J); C. caribbaea (B, E, H, K); C. tenuis sp. nov. (C, F, I, L). 358 SVEN ZEA AND ERNESTO WEIL

FIG. 4. Size of spicules of the three species at San Andre´s Archipelago (SW Caribbean, Colombia), Jamaica and Puerto Rico. Data represent specimen means ± 1 standard deviation of 25 tylostyles and 10-15 spirasters.

Marta to NW Gulf of Uraba´), San Andre´s most reef and littoral zones of all studied and Old Providence Archipelago (San An- areas, from shallow to deep (30 m) reef bot- dre´s, Providencia, Albuquerque Cays, toms. Found on rubble, bases of corals, on Courtown Cays, Serrana Bank, Roncador top of dead or live coral, and on limestone Bank, Quitasuen˜o Bank), Belize. Dubious pavement. At Islas del Rosario, absent in taxonomical and ecological records need windward reef zones, but occurs in shallow confirmation. to mid-depth lagoon and leeward settings Ecology.—Very abundant throughout (up to ca. 12 m). TAXONOMY OF CARIBBEAN EXCAVATING SPONGE 359

FIG. 5. Size of spicules of the three species at Venezuela, continental coast of Colombia and Belize. Data represent specimen means ± 1 standard deviation of 25 tylostyles and 10-15 spirasters.

Remarks.—Slide preparations made by us Cliona aprica seldom grows thick and be- from a decalcified fragment of the holotype comes riddled with epibiotic zoanthids; (YPM 8723, forma profunda)-kindly sent by a form that agglutinates rubble occurs E. Lazo-Wasem-did not contain any spic- in shallow habitats (Lo´pez-Victoria et al. ules. Therefore, we used our own material in press). At the oceanic islands and atolls from the type locality (Discovery Bay, of the SW Caribbean and in Jamaica, north coast of Jamaica) as reference to iden- this species is quite distinctive, being tify the remaining samples. dark brown to black, often with papillae 360 SVEN ZEA AND ERNESTO WEIL

FIG. 6. Comparative view of some spicule characteristics at the areas sampled. Data represent the means ± 1 standard deviation of the specimen means at each area (for number of specimens measured in each area, see Table 1). extensively fused as to be almost fully en- phology is the norm, specimens may crusting. Young, papillated specimens of be confused in the field with papillated C. C. caribbaea can be distinguished from C. caribbaea. In these cases the specimens aprica by their lighter brown color and the can be identified with certainty only larger papillae with grayish oscules. How- through analysis of spicules because C. car- ever, at the coasts of Central and South ibbaea usually has larger and stouter tylo- America, where Cliona aprica often also has styles, and slender, narrow and wavy spi- grayish oscules, and papillated mor- rasters. TAXONOMY OF CARIBBEAN EXCAVATING SPONGE 361

Cliona aprica and C. tenuis are easily dis- 350 (Grand Cayman, in part; combined with tinguished by external morphology alone. Cliona tenuis sp. nov.; vs. organic pollution); The former rarely covers the entire substra- Acker and Risk 1985: 706, fig. 3 (dark colored tum when encrusting and the latter is al- form, Grand Cayman, ecology); Scho¨nberg 2000: ways thinly and fully encrusting. They 168; 2002: 296 (referring to the type material); Lo´pez-Victoria et al. in press (Colombia, biol- have very similar wide-turning spirasters, ogy). but tylostyles of C. tenuis are generally ?Cliona caribbaea; Pomponi 1976: 572, fig. 6 smaller (Figs. 3-6). At Belize, there remains (Bahamas, Florida, ultrastructure of burrows); the possibility that what we are calling C. 1977: 485 (Bahamas, Florida, ultrastructure of aprica is a papillated C. tenuis. In this area, etching cells); 1979: 317 (Bahamas, Florida, Ja- C. tenuis often develops papillae second- maica, ultrastructure and cytochemistry of etch- arily wherever the sponge surface has been ing area); Hudson 1977: 491 (Florida, growth on smothered by sand or bitten by fish. C. corals); MacGeachy 1977: 479 (Barbados, factors aprica from Belize is not as dark as in other controlling boring); Risk et al. 1980: 376 (Costa areas, and is usually found in rubble in Rica, coral bioeroders); Buznego and Alcolado 1987: 6 (Cuba, boring on corals); Alcolado 1989: shallow bottoms, where the excess sedi- table 1 (Cuba, distribution); Schmahl 1990: 379 ment and growth of turf algae may prevent (Florida, distribution); Ru¨ tzler et al. 2000: 234 papillar fusion. Tylostyles are rather simi- (Belize, lagoon reef mangroves). lar in both cases, and although slightly Non Cliona caribbaea; Verrill 1907: 343, pl. 35d, smaller in C. tenuis, they largely overlap fig. 4 (Bermuda, proposing a new name, C. sor- (Figs. 3-5, Table 1). Spirasters are generally dida); de Laubenfels 1936a: 155 (Dry Tortugas, as of the same size and shape (Fig. 3, J vs. L), C. caribboea); 1936b: 461 (Panama, as C. carib- although spires tend to be slightly wider in boea); 1950: 108 (Bermuda, as C. caribboea); 1953a: C. tenuis (Fig. 5). These subtle spicule dif- 540 (eastern Gulf of Mexico, as C. caribboea); ferences were evident only after comparing 1953b: 22 (eastern North America, as C. caribboea) [all these are of uncertain identity, fide several sympatric specimens of both spe- Hechtel 1965: 60, Pang 1973a:22, and Ru¨ tzler cies. Transplant experiments carried out at 1974:7, and from examination of de Laubenfels’ San Andre´s (oceanic SW Caribbean) and at Bermudan material deposited at BMNH, Islas del Rosario (continental coast of Co- 1948.8.6.46]; Wells et al. 1960: 232 (North Caro- lombia) showed that C. aprica always grow lina); Little 1963:58, fig. 28 (Florida’s Gulf of papillae on new substratum, while C. tenuis Mexico coast) [the latter two records are Suberites never did (Lo´pez-Victoria et al., in press). undulatus George and Wilson 1916, fide W. D. These results led us to use the name C. Hartman in Hechtel 1965:60]; Pang 1973a: 22, fig. 5 aprica for those papillated specimens from (Jamaica, = Cliona flavifodina Ru¨tzler, 1974); Corte´s Belize that did not have the distinctively et al. 1984: 228 (Costa Rica, =Cliona tenuis); Lehnert and van Soest 1998: 79 (Jamaica, uncertain iden- narrow and wavy spirasters of C. caribbaea. tity, possibly C. flavifodina); Hofman and Kielman 1992: 215, fig. 9 (Colombia; specimen INV-POR Cliona caribbaea Carter, 1882 0406 is Cliona aprica; specimens INV-POR 0397 Pl. 1 (B, D, F), Pl. 2 (B, E, H, K). Fig. 2 (B), and 0411 are Cliona flavifodina). Fig. 3 (B, E, H, K), Figs. 4-6 Cliona langae Pang 1973a: 34, fig. 9 (Jamaica, holotype YPM 8716, 7 paratypes at BMHN and State University of New York at Stony Brook- Cliona caribbaea Carter 1882: 346. fig. 26 (St. University of the West Indies) [synonymy sug- Vincent, type at City of Liverpool Museum); gested by Ru¨ tzler 2002b, and confirmed herein]; Topsent 1889: 49 (Guadeloupe); Ru¨ tzler 1974: 5, Pang 1973b (Jamaica, ecology); Tunnicliffe 1979: figs. 2-4 (Bermuda, Dominica, Panama); 1975: 311 (Jamaica, role in coral fracture); Lehnert and 214 (Bermuda, biomass, area coverage, density); van Soest 1998: 79 (referring to the type mate- 1986: 122, fig. 33, color pl. 4.11 (Bermuda); 1990: rial). 460 (Bermuda, zooxanthellate symbionts); ?Cliona langae; Pomponi 1979: 317 (Bahamas, 2002a: figs. 5, 6F, 6G, 7C (from Ru¨ tzler 1974); Florida, Jamaica, Ultrastructure and cytochem- 2002b: 64, fig. 4.4, 4.5 (Bahamas; Belize; in part, istry of etching area); Alcolado 1999: 121 (Cuba, only some of the papillose and thickly encrust- distribution). ing, deep-water specimens); Rose and Risk 1985: Non Cliona langae; Humann 1992: 56 (Car- 362 SVEN ZEA AND ERNESTO WEIL ibbean, material identified by S. Pomponi; the 2.3 mm in diameter, scattered and conspicu- specimen pictured conforms to Cliona tenuis]. ous, usually with a creamy rim. Younger ?Cliona viridis; Topsent 1900: 84 (in part, Car- individuals may be entirely papillated; ibbean material?), pl. 3, fig. 3d [synonymy sug- fully encrusting specimens occasionally gested by Pang 1973a: 22 and Ru¨ tzler 1974: 5]. with papillae at growing edge. Tylostyles ?Cliona viridis var. caribbaea; Topsent 1932: 563, robust, with rounded to slightly elongated fig. 5 [change of name for Topsent, 1889 material]. ␮ ␮ Non Cliona viridis (Schmidt 1862) (a valid spe- heads, 271-465 m long by 4.7-14.3 m cies from the Mediterranean, Croatia); Hechtel wide. Spirasters narrowly turning, 14.9- 1965:61 (Jamaica, sinonymyzed to C. caribbaea by 47.0 ␮m long, 0.3-1.5 ␮m thick, with usually Pang 1973a: 22 which is Cliona flavifodina). more than 5-6, and up to 10 turns (but only Cliona sp. 2; Zea 2001 (SW Caribbean atolls, 5-6 at San Andre´s Archipelago); maximum distribution; in part, lagoon and deep records; width of spire 1.5-5.0 ␮m; spines up to 2 shallow windward records are Cliona tenuis.) ␮m, branched at the San Andre´s Archi- pelago, mostly unbranched elsewhere. Studied material.—Jamaica. Discovery Morphology.—Encrusting; sponge gener- Bay, Dairy Bull: 8-30 m, ICN-MHN(Po) 185, ally completely covering the excavated INV-POR 646, 647, 648, 650; Fore reef: 12-28 substratum with rather thick tissue (up to m, INV-POR 651, 652, 653, 654. Continental 1-2 mm), amber brown to gray brown coast of Colombia. Rosario Islands, San (NGC 21-Fuscous, 22-Burnt umber, 23, 223- Mart´ın, Pajarales: 18-21 m, INV-POR 655. Raw umber, 37-Drab, 32-Chestnut, 36- San Andre´s and Old Providence Archi- Amber), in places with darker grayish pelago (Colombia). San Andre´s Island, tones (19-Dusky brown, 20-Dark grayish Wildlife, 9-15 m: ICN-MHN(Po) 182, INV- brown, 21-Fuscous, 44-Smoke gray). Size POR 635, 636, 637, 638. Courtown (=Bol´ı- may range from few centimeters to about 1 var) Cays: 6-8 m, INV-POR 639. Old m in diameter. Oscules usually large (0.9- Providence Island, Blue Hole: 15-27 m, 2.3 mm) and conspicuous, frequently with ICN-MHN(Po) 183, INV-POR 640. Serrana a slightly elevated and lighter-colored col- Bank: 2.5-7 m, ICN-MHN(Po) 184, INV- lar. Surface smooth, with fields of pores in POR 641, 642, 643, 644. Quitasuenõ Bank: interoscular areas of some specimens, 0.9- 12-13 m INV-POR 645, 646. Belize. Carrie 1.5 mm in diameter, visible as lighter- Bow Cay area, North of South Water Cay: colored meshes within darker tissue. When 0.5-27 m, INV-POR 656, 657; Pelican Cays, young or in bases of corals, sponge occa- Cat Cay: 1-2 m, ICN-MHN(Po) 186. sionally papillated, papillae 0.9-3 mm in di- Other material examined.—Holotype, ameter, often fused in scattered groups or LIVCM 2177 (SEM images of spicules, having a central, fully encrusting portion. drawings and photos of preserved speci- Fully encrusting specimens in active men, also published in Scho¨nberg 2002); growth somewhat thinner (<1 mm), often USNM 24346, 24348 (Bermuda, spicule with scattered papillae at growing edges, slides of Ru¨ tzler 1974 material). BMHN papillae 0.3-1.8 mm in diameter. Specimens 1948.8.6.46 (Bermuda, mistaken record by that cannot advance further grow thicker, de Laubenfels 1950, fragment and spicule often invaded by light yellow zoanthids. slides INV-POR 631); BMNH 1973.8.21.9 Sponge penetrates and excavates 0.7-1.3 cm (Jamaica, mistaken record of Pang 1973a, below the surface. Excavated troughs in collected by H. M. Reiswig, fragment and Montastraea cavernosa coral skeleton (the spicule slides INV-POR 632); INV-POR only ones examined in cross section for 0406, 0397. 0411 (Colombia, mistaken rec- Cliona caribbaea) cylindrical, 580 ␮m-1.3 mm ords by Hofman and Kielman 1992); Holo- wide, 2.2-9 mm deep. Young specimens type of Cliona langae Pang 1973a, YPM 8716 with solid pillars of coral skeleton more or (Jamaica, spicule slides INV-POR 633). less intact, although pierced by circular ex- Diagnosis.—Thick encrustations (up to 2 cavated chambers 95-332 ␮m wide; inter- mm), growing over and completely cover- tabular coral spaces generally rectangular. ing substratum. Size up to1mindiameter. Coral pillars in older specimens strongly Amber brown to gray brown. Oscules up to eroded, much thinner and irregular. Pali- TAXONOMY OF CARIBBEAN EXCAVATING SPONGE 363 sade of tylostyle brushes covers both exca- lize in shallow rubble (papillated) and on vated troughs and substratum rims; tips of deep slopes (encrusting); in continental spicules protrude about 1/3 of their length coast of Colombia seen only in papillated above the pinacoderm, brushes often form on deep, leeward reef slopes. At SW fouled with debris. Incurrent canals, 19-76 Caribbean oceanic islands and atolls, la- ␮m wide, common in between spicule goon and leeward settings from about 3 m brushes, reaching down to subectosomal to reef slopes (ca. 30 m); in windward set- spaces and canals, 47-114 ␮m wide, more or tings on deeper reefs; most specimens en- less parallel to the surface. Thickness of crusting. Thick portion of specimen col- ectosomal area 28-285 ␮m in thin actively lected at San Andre´s on dead Montastraea growing specimens; on non-growing speci- annularis coral head on May 22, 2001, with mens may reach 220-860 ␮m. Tissue occa- eggs 114-133 ␮m in diameter, scattered sionally traversed by circular canals 28-330 throughout choanosomal tissue; thin por- ␮m in diameter. tion of same specimen lacked eggs. Eggs Spicules.—Tylostyles usually with with nucleus and a nucleolus, surrounded rounded heads, generally slightly elon- by layer of nurse cells. gated (length/width >1), half above the Remarks.—The identity of the studied neck trapezoidal in profile, upper half material was confirmed by examination of rounded; shafts robust, usually slightly spicule slides from Bermudan specimens curved. Measurements (Figs. 4-6, Table 1, described by Ru¨ tzler (1974), a drawing and range of means): length 340-379 ␮m, shaft SEM photos of the holotype spicules (made width 8.4-12.0 ␮m, head width 11.3-15.1 and published by Scho¨nberg 2002). Junior ␮m, head length 12.1-14.3 ␮m, head synonymy of Cliona langae was determined length/width 0.9-1.1 ␮m. Spirasters long, from examination of the species at Jamaica, narrowly turning, sparsely to profusely its type locality, and from the analysis spined; spines relatively short, branched in of holotype spicules. Upon examination of bouquets on material from San Andre´s Ar- the material deposited at BMNH, we con- chipelago, but with little branching else- firmed Pang’s (1973) mistaken use of the where. Most spirasters with many turns name C. caribbaea for C. flavifodina Ru¨ tzler. usually more than 5-6 and up to 10; spi- To the unaware observer, encrusting rasters with fewer turns can occur within specimens of this species can be easily con- the same specimen. At San Andre´s Archi- fused with Cliona tenuis. They are distin- pelago, most spirasters with up to 5 turns. guished by the greater tissue thickness and Measurements (Table 1, range of means): oscule size in C. caribbaea. However, some length 26.7-37.3 ␮m, shaft width 0.59-0.9 well developed specimens of Cliona tenuis ␮m; spire maximum diameter 2.1-2.8 ␮m; may be as thick as thinner C. caribbaea, and number of turns 4.3-7.6; longest spire some may show oscules with a slightly el- length 10.6-13.2 ␮m. Spine full height evated collar. Transplanted fragments of C. (min.-max.) 0.5-2.0 ␮m. caribbaea grew initially papillated in the Distribution.—Bermuda, San Salvador new substratum, while those of C. tenuis (Bahamas), Jamaica, Grand Cayman, never did (Lo´pez-Victoria et al. in press). Guadeloupe, Dominica, St. Vincent, Conti- Papillated specimens of C. caribbaea re- nental coast of Colombia (Islas del Rosario), semble C. aprica in the field, but tend to Panama, San Andre´s and Old Providence have larger papillae and a lighter colora- Archipelago (San Andre´s, Providencia, Al- tion. But some specimens of C. caribbaea in buquerque Cays, Courtown Cays, Serrana Belize had a dark brown surface and Bank, Roncador Bank, Quitasuenõ Bank), slightly larger papillae than co-occurring Belize. Dubious taxonomical and ecological specimens of C. aprica. The more robust and records need confirmation. long tylostyles, and the narrower spires of Ecology.—At northern Jamaica from the spirasters clearly distinguish this spe- about6mtoreef slope, in deeper waters cies from the other two described here. Ex- generally papillated. Not very common at cept at the San Andre´s Archipelago, where Central and South American coasts; in Be- spirasters are relatively short, all others 364 SVEN ZEA AND ERNESTO WEIL specimens have some or most spirasters Type material.—Holotype: ICN-MHN(Po) long and with 6 or more turns. On the en- 187, San Andre´s Island, Half a Reef, shal- crusting specimens of this species, the ecto- low windward fore-reef terrace, 5 m, on some is the only one where the palisade of dead Acropora palmata coral, coll. M. Lo´pez- erect spicule brushes occurs throughout the Victoria. Paratypes: Jamaica. Discovery entire surface. Bay, Dairy Bull: 7-14 m, ICN-MHN(Po) 188, INV-POR 667; Fore reef: 9 m, INV-POR 668. Cliona tenuis sp. nov. Puerto Rico. La Parguera, coastal reefs: E. Pl. 1 (C, G, H), Pl. 2 (C, F, I, L). Fig. 2 (C), Weil, INV-POR 691; El Veril: 20 m, ICN- Fig. 3 (C, F, I, L), Figs. 4-6 MHN(Po) 192, INV-POR 688, 689, 690. Continental coast of Colombia. Rosario Is- Cliona aprica;Ru¨ tzler 1975: 205 (Belize, bio- lands, Isla Grande, Canal del France´s: 5-6 erosion rates); Pulitzer-Finali 1986: 95 (Puerto m, INV-POR 670, 671; Pajarales, Majayura: Rico); Vicente 1990a: 200 (Puerto Rico, zooxan- 4.5-6 m, ICN-MHN(Po) 189, INV-POR 672, thellate symbionts); Vicente 1990b: 439, fig. 4 673, 674, INV-POR 675, 676, 677, 678. San (Puerto Rico, overgrown by other organisms); Bernardo Islands, Bajo Minalta: 5-13 m, D´ıaz et al. 1995 (San Andre´s Island, distribution; INV-POR 679, 680,M.Lo´pez-Victoria, 682; in part, p. 56, plate 4; only data from windward Tintipań: 3 m, ICN-MHN(Po) 190; Bajo Tio- settings; in other habitats it really is C. aprica). Non Cliona aprica Pang 1973a (a valid species). solda: 10 m, M. Lo´pez-Victoria, INV-POR Cliona caribbaea; Corte´s et al. 1984: 228 (Costa 681. NW Gulf of Uraba´, Cabo Tiburoń:9m, Rica, invasion of dying corals, as C. caribbea); INV-POR 578, 579; Sapzurro: 5 m, INV- Rose and Risk 1985: 350 (Grand Cayman, in POR 580. San Andre´s and Old Providence part; probably combined with the real C. carib- Archipelago (Colombia). San Andre´s Is- baea; vs. organic pollution); Acker and Risk 1985: land, Sound Bay: 1.5 m, INV-POR 659; Bo- 706, figs. 3, 5, 6 (light colored form, Grand Cay- catora Hole: 10 m, INV-POR 660; Half a man); Antonius and Ballesteros 1998: 151, figs. Reef: 4.5 m, INV-POR 661; East Reef, south: 7-8 (Belize, as epizoism; as C. caribbea); Ru¨ tzler 3 m, INV-POR 662, 663, 664. Courtown 2002b: 64, figs. 2, 3, 4.2, 4.3, 6 (in part, thinly (=Bol´ıvar) Cays: 3 m, INV-POR 665. Quita- encrusting specimens). Non Cliona caribbaea Carter 1882 (a valid spe- suenõ Bank: 1.5 m, INV-POR 666. Belize. cies). Carrie Bow Cay area, Carrie Bow Cay: 0.5-7 Cliona langae; Humann 1992: 56 (Ca- m, INV-POR 683, 684, 685, 686, 687; North ribbean, material identified by S. Pomponi); of South Water Cay: 0.5 m, ICN-MHN(Po) Williams et al. 1999: 843 (Puerto Rico, on live 191. and dead corals). Type locality.—San Andre´s Island, SW Non Cliona langae Pang 1973a; 1973b (=C. car- Caribbean Sea, spur and groove fore reef at ibbaea Carter 1882). Half a Reef, 5 m, 12°32Ј35Љ N, 81°40Ј57Љ W. Cliona aprica – C. langae – C. caribbaea species Diagnosis.—Thin, entirely encrusting ve- complex; Valderrama 2001: 32; Valderrama and neer of rather transparent brown tissue, Zea in press (morphotype 2, Gulf of Uraba´, distribution). with yellowish, greenish, reddish or orange Cliona sp. 2; Zea 2001 (SW Caribbean atolls, tones. Size up to several meters in diam- distribution; in part, only windward shallow eter. Oscules small and inconspicuous, up sites; lagoon and deep records are Cliona carib- to 1.4 mm in diameter. Tylostyles rather baea). short, with elongated heads, 199-380 ␮m Cliona sp.; Lo´pez-Victoria et al. in press (Co- long by 3.3-14.3 ␮m wide. Spirasters wide lombia, biology). turning, 11-39 ␮m by 0.5-1.3 ␮m, with usu- Anthosigmella varians forma incrustans; Leh- ally 1-4 turns; maximum width of spires 8 nert 1993: 60, Tab. 22, figs. 22, 33-35, 130-131 ␮m; heavily branched spines, up to 2.0 ␮m (Cozumel). tall; a few straight or u-shaped spirasters. ?Anthosigmella varians forma incrustans; Le- hnert and Fischer 1999: 309 (Jamaica, distribu- Morphology.—Sponge encrusts entire val- tion). ley of excavated substratum with a thin, Non Anthosigmella varians (Duchassaing and smooth tissue veneer through which the Michelotti 1864) forma incrustans Wiedenmayer underlying substratum structure is visible. 1977 [=Cliona varians, a valid species]. Valley up to 1-2 cm deep, can reach several TAXONOMY OF CARIBBEAN EXCAVATING SPONGE 365 meters in diameter, rounded when small, widely turning spires, profusely spined, irregular, amoeba-like in outline when spines relatively short, branched in bou- large. Color depends on tissue thickness, quets; ends of spirasters with elaborate density of substratum, and illumination, spination. Spirasters usually with 1-4 turns appearing greenish-brown, yellowish- although some with up to 7 turns; widest brown, reddish-brown, orange-brown or spire usually located at center, other dark chocolate brown. Sponges from spires often smaller and asymmetrical. Al- Puerto Rico, continental Colombia and Be- most straight spirasters common, a few u- lize generally maroon to dark brown. Tis- shaped. Measurements (Table 1, range of sue color of samples brought to daylight means): length 22.7-24.8 ␮m, shaft width were various shades of brown to grayish 0.7-1.0 ␮m; Spire maximum diameter 2.8- brown in the thicker portions (19-Dusky 4.3 ␮m; number of turns 2.7-4.3; longest brown, 20-Dark grayish brown, 21- spire length 11.7-16.9 ␮m. Spine total Fuscous, 22-Burnt umber, 31-Maroon, 119- height (min.-max.) 0.7-2.0 ␮m. Size of spic- Sepia), and lighter shades of brown to ules varies with locality (Table 1, Figs. 6, 7), cream in thinner portions (23-Raw umber, with tylostyles generally larger and more 26-Clay color, 54-Cream). Edges of sponges robust and spirasters thicker at continental either ragged or continuous; Belizean speci- coast of Colombia. mens occasionally with papillae at some Distribution.—Bahamas, Florida, Puerto edges, which appear to be secondarily de- Rico, Jamaica, Grand Cayman, Dominican veloped wherever sponge surface smoth- Republic, Continental coast of Colombia ered by sand or bitten by fish. Oscules (Islas del Rosario to Gulf of Uraba´ ), small (0.4-1.4 mm in diameter), inconspicu- Panama´, Nicaragua-Roatań, San Andre´s ous, without contrastingly colored collar, and Old Providence Archipelago (San An- except in some specimens at Belize with dre´s, Providencia, Albuquerque Cays, slightly elevated, transparent conical col- Courtown Cays, Serrana Bank, Roncador lars. Surface occasionally colonized by light Bank, Quitasuenõ Bank), Belize, Cozumel. yellowish zoanthids, although only seen in Localities in italics given above are from some deep-water specimens (ca. 20 m). observations by the junior author. Sponge penetrates and excavates substra- Ecology.—Cliona tenuis is abundant in tum only upper 0.6-2.0 cm. Excavated shallow (2-3 m) to mid depth (15-20 m), troughs rather narrow, up to 800 ␮m wide, wave-exposed environments, including with coral septae more or less intact (Fig. fore- and back-reef settings, littoral lime- 2C). Elevated rims of substratum covered stone cliffs and terraces. It is dominant in by a thin tissue layer. Denser substratum branches and pavement of dead and col- areas with irregular excavated chambers lapsed Acropora palmata reef zone in many and tunnels, 140 ␮m-1 mm wide. Incurrent localities throughout the Caribbean and canals, 23-57 ␮m wide, occur in between abundant in deep windward terraces of some ectosomal spicule brushes and open SW Puerto Rico (ca. 20 m). Widespread in below into subectosomal spaces. Choano- windward fore-reef terraces of SW Ca- somal tissue rather dense, with few and ribbean islands, atolls and banks, but ab- small canals, 28-465 ␮m wide. sent at similar sites in Serrana Bank (San Spicules.—(Fig. 4C, F, I, L; 5C, F, I, L) Ty- Andre´s Archipelago, Colombia) and Los lostyles, many with elongated heads Roques Archipelago (Venezuela). (length/width >1), half portion above neck Etymology.—From Latin tenuis, meaning trapezoidal in profile, upper half rounded; thin; referring to the thinness of the tissue shafts rather short, robust or thin, slightly through which the structure of excavated curved; when robust, neck is wide. Mea- substratum can be seen. surements (Figs. 4-6, Table 1, range of Remarks.—Of the three species described means): length 246-308 ␮m, shaft width 5.6- here, Cliona tenuis has re-colonized freed 9.4 ␮m, head width 9.2-12.4 ␮m, head substratum after the massive die-off of ac- length 9.3-12.9 ␮m, head length/width 1.0- roporid corals from disease and bleaching 1.1 ␮m. Spirasters, relatively short, with in the early 80’s (Corte´s et al. 1984; Acker 366 SVEN ZEA AND ERNESTO WEIL and Risk 1985; Antonius and Ballesteros Cliona tenuis at Jamaica while we frequently 1998; Williams et al. 1999; Ru¨ tzler 2002b). It encountered it in 2002 in shallow littoral is different from C. aprica by the external terraces and in the Elkhorn coral rubble morphology and color. The spirasters are zone in fore reef settings. From her descrip- rather similar: widely turning spires and tions of C. aprica and C. langae, and analysis profusely spined; the tylostyles are smaller, of type material, it is clear that the new but only slightly at Belize (see remarks for species was not mistakenly included within C. aprica). From its external morphology, it neither of them. Perhaps the species was may be confused with fully encrusting C. uncommon or absent in the late 60’s when caribbaea; however, when they are com- Pang did her work, and when the Elkhorn pared side by side the differences are clear. coral was healthy and dominant. The problem was and remains that these The above remarks may support one of two species seldom co-exist in the same our hypotheses, viz., that Cliona tenuis is an habitat. The two species are separated by introduced species whose source may be C. studying their spicules: C. caribbaea possess orientalis. Pione lampa (de Laubenfels, 1950), rather large and stout tylostyles, and the is a bright vermilion red, thinly encrusting spirasters are narrowly turning, usually clionaid, which seems to have been intro- longer and possess more turns. In contrast duced to Bermuda from the Indo-Pacific to the other two species, C. tenuis trans- sometime before the 1950’s (Ru¨ tzler 2002b). planted fragments always grow fully en- C. tenuis has been at the San Andre´s Island crusting, although the edges may be ragged fore-reef terrace at least since 1970. If C. ori- and with bits of tissue unconnected to the entalis was introduced to the Caribbean, main body. this occurred before 1970 and from an The only other clionaid of similar color original population with a spicule comple- and habit to Cliona caribbaea and C. tenuis is ment somewhat different to that from the C. orientalis Thiele (1900), which is a com- GBR. Perhaps the apparent absence of C. mon and widespread species of the Great tenuis from east of Puerto Rico, throughout Barrier Reef, Australia (Scho¨nberg 2000; the Lesser Antillean arc, to Santa Marta in Scho¨nberg and Wilkinson 2001). We ob- South America may be related to barriers of served C. orientalis at Heron Island in the dispersion after its introduction. More de- Great Barrier Reef, and the similarities are tailed studies of specimens of C. tenuis col- obvious. Scho¨nberg (2000) described tylo- lected in the Caribbean earlier than 1970, styles similar in size and shape, but spi- and a molecular systematic analysis would rasters are more narrowly turning. Exami- help to solve this problem. nation of a specimen fragment from Heron The specimens of Cliona varians forma in- Island (INV-POR 658) showed similar tylo- crustans described and illustrated by Leh- styles size (252-299 ␮m × 4.7-6.2 ␮m, length nert (1993 as Anthosigmella) from Cozumel, by width), but smoothly elongated, drop- seem to belong to Cliona tenuis. Some of the shaped, and irregular heads; spirasters are specimens photographed look thick and on average longer (29-35 ␮m), with nar- riddled with zoanthids, typical of old C. rower spires (3-4 ␮m) sparse spination. C. caribbaea; their tylostyles size (190-290 ␮m orientalis spirasters mostly have 3-6 turns long, 3-10 ␮m wide) and shape (Lehnert’s while in C. tenuis there are many with 1-3 Figs. 130 and 131), closely conform to C. turns. Also, C. orientalis tissue penetrates tenuis. The sponge pictured on Fig. 22 is more deeply and uniformly into the sub- more like C. varians. stratum: up to 1.9 cm in our specimen from a Porites head and up to 3 cm in those cited Key to species of brown, encrusting by Scho¨nberg (2000). Tissue fills up the Caribbean clionaids skeletal coral pores, and sparse chambers were up to 1 mm in diameter. C. orientalis 1- Spirasters long, some surpassing 40 falls outside of C. tenuis spiculation varia- ␮m, and narrowly turning; maxi- tion. mum spire diameter 3.5 ␮m; with- Pang (1973a, 1973b) did not notice or find in a single specimen there are al- TAXONOMY OF CARIBBEAN EXCAVATING SPONGE 367

ways some spirasters with many elsewhere. Papillated forms of C. aprica and turns, 6 or more; encrusting or pa- encrusting C. tenuis are similar in color and pillated ------Cliona caribbaea spiculation in Belize -although comparison 1- Spirasters shorter, up to 39 ␮m, and of neighboring specimens show differ- many widely turning; spire diam- ences-, but are different elsewhere in the eter reaches 5 ␮m or more ------2 Southern Caribbean. 2- Papillated; if encrusting, seldom The geographical distribution and the lo- covers the entire substratum; brown cal co-occurrence (sympatric vs. allopatric) black ------Cliona aprica of brown clionaids are also puzzling, and 2- Fully encrusting, not papillated, until all dubious records are clarified and various shades of brown, but not areas re-visited, the picture is far from com- black ------Cliona tenuis plete. Of the three species studied, Cliona aprica is apparently the only that occurs in southeastern Caribbean, from Los Roques GENERAL DISCUSSION AND CONCLUSIONS in Venezuela, through The Netherlands Antilles, to Santa Marta in continental Co- From subtle but consistent differences in lombia, and it is absent from Puerto Rico. In external and spicule morphology, size and the Lesser Antilles, from Guadeloupe to St. observations from transplant experiments, Vincent, the only species known is C. carib- we conclude that there are three distinct baea, and it is papillated (see Ru¨ tzler 1974). species of brown to brown-black encrusting Hence, the apparent presence of only pa- and excavating sponges in the Caribbean. pillated forms of this complex from Guade- In the three species, the greater spicule size loupe to Santa Marta, including Barbados occurs in southern Colombia, as in many (F. Parra pers. obs.) may indicate the occur- other sponges; possibly related to local en- rence of a single species. If they are what richment of silica from river runoff (see Zea we named C. aprica, this species will fall 1987). But the overall differences, of the into the synonymy of C. caribbaea, and C. three species, in spicule size and morphol- langae will recover its status of valid spe- ogy are generally maintained indepen- cies. Given these taxonomical implications, dently of the locality: tylostyles are stouter further observations and sampling in the and longer in Cliona caribbaea, intermediate Lesser Antilles is needed. in C. aprica and smaller in C. tenuis; spi- The examples given above may imply rasters tend to be longer, have many turns that the taxonomical resolution of the com- and the spire is generally narrower in C. plex presented here is incomplete and that caribbaea (Table 1, Figs. 4-7). Nevertheless, there may be more un-described cryptic some spicule characteristics, within each species or local predominant phenotypes species, vary with geographical location: C. are genetically fixed. A molecular sys- aprica tylostyle heads are blunt (head tematic analysis is needed to clarify these length/width <1), in comparison with the issues, but a careful comparison of co- other two species, at San Andre´s, Jamaica occurring specimens is necessary to recog- and the continental coast of Colombia, but nize the similarities and differences be- are greatly elongated at Venezuela; C. ca- tween the species in a given geographical ribbaea tylostyle heads are usually elon- locality. gated, but at Bermuda they are blunt We have not included Cliona varians (Du- (Ru¨ tzler 1974); spirasters of C. caribbaea chassaing and Michelotti) in this “com- usually have more turns than the other spe- plex” of Caribbean clionaids, as it was de- cies, except at San Andre´s (Table 1, Fig. 8). scribed before and it is distinguished by its: The predominant external morphology (pa- thicker (up to 1-2 cm) external tissue, light pillated, encrusting) of the studied species amber color, tylostyle shape, and the u- also varies geographically. For example, shaped spirasters (see also Scho¨ nberg Cliona caribbaea is mostly papillated in Ber- 2002). In contrast to the group of species muda and the Central and South American studied here (see Lo´pez-Victoria et al. in coasts, while predominantly encrusting press), C. varians seem to overgrow the 368 SVEN ZEA AND ERNESTO WEIL substratum before excavating it (Vicente Cliona caribbaea on Grand Cayman Island. J. Sedim. 1978) and it does not use pioneering tissue Petrol. 55:705-711. threads to undermine coral polyps (S. Zea Antonius, A., and E. Ballesteros. 1998. Epizoism: a new threat to coral health in Caribbean reefs. Rev. and M. Lo´pez-Victoria, unpublished obser- Biol. Trop. 46:145-156. vations). Alcolado, P. M. 1976. Lista de nuevos registros de po- r´ıferos para Cuba. Acad. Cienc. Cuba, Inst. Oceanol. Acknowledgments.—Sampling in Colom- Ser. Oceanolog´ıa 36:1-11. bia funded by the Colombian Science Fund Alcolado, P. M. 1979. Estructura ecolo´gica de la comu- (COLCIENCIAS, grants 30003-1-33-81, nidad de esponjas de un perfil costero de Cuba. 30003-154-83, 2105-09-023-93, 2105-09-120- Cien. Biol. 3:105-127. 97 and 110109-10387, to S. Zea and J. M. Alcolado, P. M. 1989. Estructura ecolo´gica de las comunidades de esponjas del arrecife de Rincońde D´ıaz), and with matching funds from IN- Ganabo, Cuba. Rep. Invest. Inst. Oceanol. 10:1-16. VEMAR, Universidad Nacional de Colom- Alcolado, P. M. 1990. General features of Cuban bia and University of Puerto Rico (last sponge communities. In New perspectives in sponge grant only). Sampling at Puerto Rico was biology, ed. K. Ru¨ tzler, 351-357. Washington, DC: funded by University of Puerto Rico Sea Smithsonian Institution Press. Grant Program (to E. Weil). Sampling at Alcolado, P. M. 1999. Comunidades de esponjas de los Belize was partly funded by Smithsonian arrecifes del archipie´lago Sabana-Camagu¨ ey, Cuba. Bol. Invest. Mar. Cost. 28:95-124. Institution’s Caribbean Coral Reef Ecosys- Buznego, M., and P. M. Alcolado. 1987. Frecuencias de tem Program—CCRE. Sampling at Jamaica, ataques de esponjas perforadoras sobre algunos Belize and Curaçao was funded under corales escleract´ıneos y otros sustratos marinos en grants from COLCIENCIAS (1101-09-11241 Cuba. Rep. Invest. Inst. Oceanol. 59:1-18. to S. Zea) and from the Netherlands Foun- Corte´s, J., M. Murillo, H. M. Guzmań, and J. Acunã. dation for the Advancement of Tropical Re- 1984. Pe´rdida de zooxantelas y muerte de corales y otros organismos arrecifales en el Caribe y Pac´ıfico search—WOTRO (WB 82-261 to R. W. M. de Costa Rica. Rev. Biol. Trop. 32:227-231. van Soest). Logistic support was provided D´ıaz, J. M., J. Garzoń-Ferreira, and S. Zea. 1995. Los by R. Vieira’s CEINER Oceanarium (Islas Arrecifes coralinos de la isla de San Andre´s, Colombia: del Rosario), Fundacio´ n Cient´ıfica Los estado actual y perspectivas para su conservacioń. 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