Caribbean Journal of Science, Vol. 39, No. 3, 348-370, 2003 Copyright 2003 College of Arts and Sciences University of Puerto Rico, Mayagu¨ez 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.