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Impact of Crustose Clionid Sponges on Caribbean Reef Corals

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Impact of Crustose Clionid Sponges on Caribbean Reef Corals ACTA GEOLOGICA HISPA ICA, v. 37 (2002). n' I, p. 61-72 Impact of Crustose Clionid Sponges on Caribbean Reef Corals K. ROTZLER (I) (1) Departmenr oflnverrebrale Zoology. Narional Musellm ofNorural History. Smithsonian Insrirution. Washington. D.C. 20560-0163. US.A. Fax: 2023573043. E-mail: [email protected] ABSTRACT Some species of limestone-excavating Porifera (Clionidae, Hadromerida) cover their substrate as a thin, continuous, veneer-like crust (beta stage). This film oftissue is the result of fusion ofthe initially discrete incurrent and excurrent papillae (alpha stage) that are the common and lifelong morphological feature of most other representatives of the family. In the tropical and subtropical western At­ lantic, at least four species ofclionids encrust reef-coral skeletons (Scleractinia, Hydrozoa): Cliona caribbaea CARTER (including C. aprica PANG and C. langae PANG), C. delilrix PANG, C. lampa de LAUBENFELS, and C. varians (DUCHASSAING and MICH­ ELOTTI) (=Anthosigmella varians of authors). One conspicuous feature of these encrusting sponges is that many border live coral or cover recently dead coral as indicated by the clear outline of the coral calicular structure under the thin sponge veneer. Field experi­ ments and histological study conducted on Cliona caribbaea in Belize and Cliona lampa in Bermuda indicate that the sponges over­ power stressed coral which they overgrow at a fast rate. Stress parameters include extended periods of above-average water warming or below-average water cooling, excess of suspended sediments, organic pollution, and physical damage inflicted hy fish bites, an­ chors, and other means. Clionids do not seem to produce toxic compounds that affect virile coral colonies and are repelled hy healthy coral polyps. Overgrowth is accomplished by excavating coral calyces from below the surface, thus depriving the polyps of their sup­ pon, or by covering skeletons ofdying coral. Overpowering corals hy bioerosion is a successful competitive mechanism that works al­ so on unstressed coral, albeit at a much slower pace. On the other hand, also non-boring encrusting sponges may overgrow coral by lateral spreading, for instance the symbiotic (with cyanobacteria) species of Chondrilla and Terpios, panicularly if sponge growth is stimulated and coral resistance weakened by elevated levels of pollution. There are indications that encrusting clionids and other sponges may dramatically change the community structure and physical stability ofshallow reefs that are readily compromised by nat­ ural or anthropogenic pressures. Keywords: Sponges. Clionidae. Corals. Competition. Bioerosion. Reefs. Caribbean. 61 K.ROTZLER RESUMEN Algunas especies de esponjas perforantes de carbonatos (Clionidae, Hadromerida) cubren el substrato calcareo como una costra del­ gada y continua, similar a un revestimiento (estadio beta). Esta pelicula de tejido es el resultado de la fusion de las inicialmente ais­ ladas papilas incurrentes y excurrentes que son la caracteristica morfologica comun y de mayor longevidad de muchas otras repre­ sentantes de la familia. En el Atlantico occidental tropical y subtropical, por 10 menos cuatro especies de clionidas incrustan los esqueletos del coral arrecifal (Scleractinia, Hydrozoa): Cliono caribbaea CARTER (incluyendo e. aprica PANG y e. tangae PANG), e. delitrix PANG, e. tampa de LAUBENFELS, y e. varians (DUCHASSAING y MICHELOTTI) (=Anthosigmella varians de los au­ tores). Un caracter conspicuo de estas esponjas incrustantes es que muchas ribetean el coral vivo 0 cubren el coral recien muerto, co­ mo queda indicado por el contomo claro de la estructura de coral calicular bajo el fino revestimiento de la esponja. Los experimen­ tos de campo y el estudio histologico sobre Cliona caribbaea en Belize y Cliona tampa en Bermudas muestran que las esponjas dominan el coral que se encuentra bajo estres, creciendo sobre el a una velocidad rapida. Los parametros de estres incluyen periodos amplios de aguas con temperaturas tanto por encima como por debajo de la media, exceso de sedimentos en suspension, contaminacion organica, y lesiones fisicas infligidas por mordiscos de peces, anclas u olros medios. No parece que las clionidas produzcan compo­ nentes toxicos que afecten las colonias coralinas vigorosas y los polipos coralinos sanos las repelen. EI sobrecrecimiento se lleva a cabo mediante la excavacion en los calices coralinos desde debajo de la superficie, privando de esta manera a los polipos de su so­ porte, 0 cubriendo los esqueletos de coral muerto. EI ataque a los corales mediante bioerosion es un mecanismo competitivo eficaz que funciona tambien en corales no eslresados, si bien a un ritmo mucho mas lento. Por otra parte, las esponjas no perforantes tam­ bien pueden sobrecrecer el coral por expansion lateral, como hacen por ejemplo las especies simbiontes (con cianobacterias) de Chon­ dril/a y Terpios, en especial si los niveles de contaminacion altos estimulan el crecimiento de la esponja y reducen la resistencia del coral. Existen indicios de que las clionidas incrustantes y otras esponjas pueden cambiar drasticamente la estructura de la comunidad y la estabilidad ftsica de arrecifes someros que facilmente se yen comprometidos por presiones naturales 0 anlropogenicas. Patabras clave: Esponjas. Clionidae. Corales. Competicion. Bioerosion. Arrecifes. Caribe. INTRODUCTION CARTER [Pang, 1973 (as C. langae, C. apriea); Riitzler, 1974]; Mediterranean C. nigrieans (SCHMIDT) (Riitzler, Sponges are an important component of coral-reef 1973; Bavastrello et aI., 1996); C. delitrix PANG (Pang, communities, particularly in the Caribbean Sea where 1973; Rose and Risk, 1985); C. tampa de LAUBENFELS their diversity is estimated at about 600 species (Riitzler, (de Laubenfels, I950a, b; Neumann, 1966; Riitz1er, 1975); 1978; Diaz and Riitzler, 200I). On many reefs, sponges and C. varians (DUCHASSAING and MICHELOTTI) exceed hermatypic corals (including Milleporina, Sclerac­ (Wiedenmayer, 1977; as Anthosigmella varians forma in­ tinia, and OctocoraJlia) also in biomass (ashless dry erustans; Vicente, 1978; as A. varians). A few species, for weight; see Riitzler, 200I) although many surveys using instance Cliona eelata GRANT and C. nigrieans (often re­ point-count or projected-area measurements underesti­ ferred to as massive C. viridis SCHMIDT) exhibit the mate their abundance. Among them is a large number of massive (and often very large) gamma stage, particularly limestone-excavating sponges (Goreau and Hartman, in specimens found on volcanic bottoms after the original­ 1963), the majority belonging to the family Clionidae ly bored piece ofcalcium carbonate substrate is destroyed (Hadromerida), which are easily overlooked by divers be­ (Sara and Vacelet, 1973). cause they have a cryptic habit, filling chambered tunnels that they excavate in limestone rock with only small in­ During past surveys of Bermuda and Belize reefs I current and excurrent papillae «1-5 mm diameter, de­ made several studies on systematics, biology, and ecology pending on species) showing at the substratum surface. ofclionid sponges (e.g., Riitzler, 1974; Riitzler, 1975; Riit­ zler and Macintyre, 1982) which led to the observation of It is a well-known fact that some species ofClionidae a substantial recent increase ofencrusting forms and ofits exhibit encrusting (beta stage) and massive (gamma stage) detrimental effect on large reef-building corals. The pre­ growth forms (the papillate form is termed alpha stage) sent contribution analyzes the available information on en­ (Vosmaer, 1933). The beta stage is the result of laminar crusting Clionidae and examines excavation mechanisms, growth that starts with the fusion ofpapillae; it appears to growth rates, and environmental conditions that affect be genetically induced as it is not evident but in a small space competition between these sponges and corals' o'n number of Atlantic species, such as Cliona earibbea shallow Caribbean reefs. 62 Acta Geol. Hisp., v. 37 (2002), n° I, p. 61-72 Clionidae on Recent Corals ( SQuth.Water Cay Carrie Bow cay . J • STUDY SITE /' Carrie Bow Cut .lagOOn Piltti) R~!l . o 1 km . a Belize c Bermuda Figure 1. Study locations in Belize and Bennuda. (a) Carrie Bow Cay on the barrier reefofBelize; (b) locator map; (e) Bennuda inshore waters. LOCATIONS, MATERIAL AND METHODS cently dead coral (Fig. 2). The other clionids with beta growth in the area are C. varians on nearby back reefs The principal location for this study is the Smithson­ and C. de/itrix on the fore reef below 15 m; neither ap­ ian Institution's Carrie Bow Marine Field Station on the pears to have recently increased in dominance. barrier reef of Belize. Observations from Bermuda 2 (without experimental support at this time) are included The study reef covers about 3,000 m and ranges in depth from 0.5 m to 8 m. It is primarily composed ofthe for comparison because they point to a similar phenom­ stony corals Acropora pa/mata, Montaslraea annu/aris, enon ofspace competition between sponge and coral but Dip/oria /abyrinlhiformis, D. slrigosa, and Agaricia involve a different sponge species (not found in Belize) tenuifo/ia, and the hydrocoral Millepora comp/anala. As­ and a cooler climatic regime. sociated large demosponges in this high-energy environ­ ment are Chondrilla cf. nucu/a, an extensively encrust­ ing, non-boring species, massive and tough /rcinia felix, Belize and tubular, flexible Cal/yspongia vaginalis. A shallow section «5 m) of the Belize barrier reef fringing the southern
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