Issn 1198-6727

Sponges represent one of the most diverse benthic faunal groups in subtidal habitats of Caribbean coral reefs and mangroves. On coral reefs, sponges (100-261 species) surpass the species richness of other conspicuous reef organisms, such as octocorals (60-80 species) and scleractinian corals (50-60 species). In the past 35 years, researchers supported by the Caribbean Coral Reef Ecosystems program (Smithsonian Institution) have produced more than 125 publications about marine sponges. These studies have covered many disciplines, including traditional morphological descriptions of new species, but also developmental biology, ecology, symbioses, disease, and evolutionary analyses revealing population affinities throughout the Caribbean using DNA fingerprinting. Various studies have shown that the Belizean corals reefs and mangroves harbor the third richest sponge fauna in the greater Caribbean (after Cuba, and the Florida peninsula). Comparisons between reef and mangrove faunas show that, throughout the Caribbean, they are consistently distinct in their species composition. Many more species will be discovered once the less accessible habitats, such as mesophotic reefs and deeper hard bottoms, are explored. The importance of sponges as a marine resource in Belize is substantial, with respect to services relevant to both their own communities and the human domain. First, they are well known as unique biological pumps and filters, due to great living biomass combined with high water filtration capacity (up to 1 liter per cubic-centimeter sponge per hour), and to complex bacterial assemblages living symbiotically in their bodies (cyanobacteria, nitrifying bacteria, archaebacteria). Secondly, a varied morphologic diversity (shape and color), some with large sizes (up to several meters in diameter), makes them one of the most attractive and intriguing creatures to the curious sport diver visiting Belizean coral reefs. Some sponges are the main dietary component for marine turtles, and a food supplement for many reef fishes (butterfly fishes, angelfishes). Besides their nutritional benefit to sea turtles and fishes, they also provide habitats to hundreds of species of invertebrates and fishes living in cavities inside sponges. In mangrove habitats, too, we have found that sponges are diverse and abundant, particularly on stilt roots of red mangrove lining the tidal channels, and that they probably have developed a long-standing relationship with these plants, offering protection from root borers and possibly exchanging nutrients with them. Besides their attractiveness to underwater tourism, sponges, together with algae and bacteria, are among the marine organisms with highest pharmacological potential for human use, mainly from secondary metabolites produced as defensive chemicals. This well-known capacity makes them a unique resource that must be protected for the future benefit of marine as well as human communities. INTRODUCTION While oceans harbor approximately 80% of animal life on the planet, the Caribbean contains the greatest concentration of species in the Atlantic Ocean and is a global-scale hot spot for marine Biodiversity (Roberts et al., 2002). The Caribbean Sea is a semi enclosed basin of the western Atlantic Ocean, with an 1 Cite as: Diaz, M.C., Rützler, K., 2011. Biodiversity of sponges: Belize and beyond, to the greater Caribbean. In: Palomares, M.L.D., Pauly, D. (eds.), Too Precious to Drill: the Marine Biodiversity of Belize, pp. 57-65. Fisheries Centre Research Reports 19(6). Fisheries Centre, University of British Columbia [ISSN 1198-6727]. Biodiversity of sponges, Diaz and Ruetzler 58 area of about 2,754,000 km2, bathed by currents that enter through the Lesser Antilles and the Windward Passage, and leave northwesterly towards the Gulf of Mexico to form the Gulf Stream. The most prominent marine ecosystems in the Caribbean are sea grass beds (66,000 km2), coral reefs (26,000 km2), and mangroves (11,560 km2) (Miloslavich et al., 2010). Coral reef and mangrove ecosystems are among the most productive and biodiverse tropical marine communities. Coral reefs harbor 4-5% of all known species and are responsible for the highest recorded oceanic productivities (1,500-5,000 gC·m-2·year-1). Mangroves forests line as much as 60-75 % of tropical coasts and may constitute ‘biodiversity hotspots’ themselves (Rützler et al., 2000), which have been demonstrated to increase reef fish productivity (Mumby et al., 2007). In recent decades, these ecosystems have suffered the consequences of uncontrolled human development (waste water pollution, habitat destruction, clear cutting, among others), and global warming. The area coverage of mangrove has decreased about 1% per year since 1980 (Agard et al., 2007), while live coral coverage has decreased 80% during the last two decades (Gardner et al., 2003; Wilkinson, 2004). Therefore, these ecosystems and the organisms within them are not in their prime conditions and must be studied to understand their role and function and preserved if we intend for the next human generations to continue benefitting from them. Sponges may represent the most diverse benthic faunal component on Coral Reef and mangroves in the Caribbean (Figure 1). Reef sponges may reach four times the diversity of hard and soft corals (Diaz and Rützler, 2001), and mangrove sponges may equal or surpass the richest groups of macroalgae and ascidians, representing from 10 to 70% of the total root epiphytic diversity in various Caribbean sites (Diaz and Rützler, 2009). Marine sponges are essential to the ecology of these systems, mainly owing to their high capacity of water filtration and their role in metabolic processes, including those of their microbial associates (Diaz and Rützler, 2001; Lesser, 2006; de Goeij et al., 2008). In 1972, the Smithsonian Institution’s Caribbean Coral Reef Ecosystems Program (CCRE) established a field station on Carrie Bow Cay, a tiny sand islet off southern Belize formed by reef-crest debris, to provide year-round support for research by varied experts concerned with investigating biodiversity in the broadest sense, developmental biology, species interaction, oceanographic and carbonate-geological processes, community development over time, starting in the Pleistocene, and distributional, physiological, and chemical ecology. Early on, program participants consisted of staff of the National Museum of Natural History, but eventually, despite financial constraints, collaborators were brought in from other academic institutions worldwide. Numerous studies examined the biological and geological role of Porifera in the reef communities. At last count, 113 researchers focused on sponges of the Carrie Bow area, with 88 (78%) conducting fieldwork and the remainder coauthoring publications. Of the fieldworkers, 63 (72%) studied sponges directly, while the rest (25 or 28%) dealt with sponge associates. To date, 125 scientific papers have been published on the results of this research, while many more are in progress (Rützler, 2011). The present paper reviews our understanding of marine sponges in Belize and beyond to the greater Caribbean. We intend to reflect on the importance of these organisms to the marine communities they inhabit and to the human domain. MATERIAL AND METHODS We carried out a historical review of research in marine sponge biodiversity from Belize and the Caribbean from the early 1800s to the present using a comprehensive taxonomic list that contains classification and authorship information for all sponge species described for the Caribbean (Diaz, van Soest, Rützler and Guerra-Castro, in progress) The list can be found in the World Porifera database: http://www.marinespecies.org/porifera/ (Van Soest et al., 2010), or on the Porifera Tree of Life (PorToL) website (http://www.portol.org/resources). We compiled our own data and published data from other authors and summarized information about the ecological role and pharmacological use of tropical marine sponges, updating our previous review (Diaz and Rützler, 2001). Too Precious to Drill: the Marine Biodiversity of Belize, Palomares and Pauly 59 Figure 1. Sponges are conspicuous components of coral reef and mangrove fauna. (Left) Neofibularia nolitangere (brown mounds) and Callyspongia plicifera (light bluish-gray tube) on a patch reef near Carrie Bow Cay, Belize. (Right). Three common mangrove species, Mycale magniraphidiphera (translucent), M. microsigmatosa (orange), and Haliclona manglaris (light green) covering red mangrove (Rhizophora mangle) rootlet tips in a tidal channel at Twin Cays. RESULTS AND DISCUSSION Porifera biodiversity in time From the earliest descriptions by P.S. Pallas and J.B. Lamarck (mid-1700s and early 1800s) to the present, approximately 100 authors have contributed taxonomic descriptions of some 800 species of sponges from the greater Caribbean (Figure 2). The earliest comprehensive study of Caribbean sponges, published in 1864 by P. Duchassaing and G. Michelotti, dealt exclusively with collections from the Lesser Antilles, and included approximately 43 species. Subsequent work by J. S. Bowerbank, H. J. Carter, A. Dendy, O. Schmidt, and E. Topsent between 1858 and 1890 covered mainly the Gulf of Mexico and the West Indies, and added more than 150 species. The most prolific authors were the Austrian naturalist Oscar Schmidt, who contributed more than 165 species in 1870-80, and the North American Max Walker de Laubenfels who contributed more than 60 species during 1932-1954 (see Wiedenmayer, 1977 for literature review). The first sponge known from Belize (then British Honduras) was a tiny (5x12 mm) Polymastia biclavata (now genus Coelosphaera), sent to England by a local collector and described by B.W. Priest before the Quekett Microscopical Club of London in 1881. This remained the only record from Belize for the next 56 years, until the British Rosaura Expedition of 1937/38 collected five species from Belize City harbor and Turneffe Island atoll; even those specimens were not described until M. Burton’s treatise in 1954. When the participants of the CCRE program (Smithsonian Institution, National Museum of Natural History) arrived in Belize in the early 1970s, studies centered on systematics and faunistics, including the quantitative distribution of benthic organisms among the various shallow-water habitats (reachable with scuba diving). Over the next 30 years or so, taxonomy was approached by methods ranging from basic morphology to fine structure, DNA barcoding, and ecological manipulations. One highlight of these years was a workshop for six experts on Caribbean Porifera held at Carrie Bow Cay in 1997. CCRE studies have identified 30 new species, many as part of taxonomic revisions, local or Caribbean-wide, for instance of Biodiversity of sponges, Diaz and Ruetzler 60 the families Clionaidae, Mycalidae, Chalinidae and Axinellidae, and the genera Lissodendoryx (Coelosphaeridae) and Iotrochota (Iotrochotidae). Several species first described from Belizean mangroves were later found distributed on mangroves Caribbean wide. Until now, 189 sponge species have been reported from Belize reef and mangrove habitats (Diaz et al., in progress) This number represents only part of the diversity because many species that we collected remain unclassified and enigmatic and several prime sponge habitats remain unexplored for logistical reasons, such as the deep (below scuba) forereef, mesophotic bottoms, and cryptic environments. Experts estimate than once many regions, depths and habitats get explored, sponge biodiversity might nearly double, from the approximately 10,000 species recognized worldwide so far. The cumulative curve of number of species described per year in the greater Caribbean (Figure 2) shows that the sponge diversity in this region is still underestimated, and that whenever new geographic areas or different habitats are explored, undiscovered species are encountered. Such is the case of the recent description of thirteen new species from sciophilous habitats (cryptic areas of reefs, caverns, or small caves) from Curaçao and Colombia (Van Soest, 2009). Sponges are the most species-rich benthic animal group (165-265) in Cuba, Belize, and Jamaica, a higher diversity than elsewhere in the Caribbean (Miloslavich et al., 2010). Belizean sponges (189 species) represent the third most diverse fauna in the greater Caribbean after Cuba (265 species) and South Florida with (228 species; Diaz et al., in progress.). Comparing the diversities of five important marine animal groups (mollusk, crustaceans, echinoderms, corals and sponges) from 17 countries within various Caribbean marine ecoregions, Miroslavic et al. (2010) found that Belize ranked seventh in species richness. But, when they related species richness to the coastal area of each country, Belize ranked the fourth richest country, with 248 species/100 km, after Cayman islands (388 species/100 km), Costa Rica (362 species/100 km), and Puerto Rico (262 species/100 km). Porifera in the Caribbean and habitat preservation A classical approach to species conservation is to preserve the habitats where they live. This approach becomes even more critical when the species have specific habitat preferences. Scientists, park managers, or government officials might wonder how distinct mangrove and reef faunas are, and which habitat might be more important to protect. We have found that despite geographic contiguity between both habitats, their sponges present biological distinctness, which shows the importance of preserving both ecosystems. Diaz (in press) compared mangrove and coral reef sponge species composition in four distant Caribbean regions (Belize, Cuba, Panama, and Venezuela) and showed that the compositions of these faunas were statistically different. The taxonomic distinctness among faunas was observed at various supraspecific levels (genera, families). For example, major reef players such as species in the family Petrosiidae (genera Xestospongia, Neopetrosia, Petrosia), the family Agelasidae (Agelas spp.) and the order Verongida (Aplysina, Verongula), are basically absent from contiguous sponge-rich mangrove communities. On the other hand, the family Chalinidae (Haliclona, Chalinula) and the family Mycalidae (Mycale spp.) are more species-rich in mangroves than on coral reefs. It is assumed that differences might reflect distinct histories for both faunas. These results place in evidence the need to preserve both ecosystems in order to protect such distinctive faunal components. Figure 2. Cumulative number of sponge species described in the Caribbean from 1766 to the present. Too Precious to Drill: the Marine Biodiversity of Belize, Palomares and Pauly 61 Ecosystem services Biological pumps Vast volumes of water (up to 1 liter·cm-3 sponge tissue per hour) can be pumped and filtered by marine sponges (Reiswig, 1974). Estimating the biomass of sponge populations in three reef types in Belize, Wilkinson (1989) found the highest values (in wet weight) on inner (lagoon) reefs (1,011-2,458 g·m-2), followed by barrier back reefs (99-1354 g·m-2), and outer reefs (368-702 g·m-2). Assuming an average daily pumping activity of 12 hours (Pile et al., 1997), and a wet volume to weight ratio for sponge tissue of 0.5 (Corredor et al., 1988), we can extrapolate that sponges in Belize reefs may pump 59414,748 l water m-2·day-1. This large capacity of water filtration makes sponges not only filter feeders par excellence (Vacelet and Boury Esnault, 1995) but—owing to animal and microbial metabolic processes referred to below—gives these animals a unique role in water transformation with unprecedented ecological consequences. For example, sponges are well known to have high removal rates of particular organic carbon (POC; Reiswig, 1971; Richter et al., 2001; Scheffers et al., 2004) and even higher rates (up to two orders of magnitude) of removal of bulk dissolved organic carbon (DOC; Yahel et al., 2003; de Goeij and van Duyl, 2007). De Goeij et al., (2008) conclude that the three Caribbean thinly encrusting sponges Halisarca caerulea, Merlia normani, and Mycale microsigmatosa, are dissolved organic matter (DOM)feeders and thus act as sinks of DOC on the reefs they inhabit. The microbial processes of nitrification (aerobic transformation of ammonium to nitrite and nitrate) and denitrification (anaerobic reduction of nitrate to nitrogen gas) have been shown to occur among Caribbean and Mediterranean sponges, and project the highest benthic nitrification rates in tropical waters (Diaz and Ward, 1997; Southwell et al., 2007; Schläppy et al., 2010). Therefore, sponge population size and composition could strongly influence the concentration and speciation of dissolved inorganic nitrogen (DIN) in the reef and mangrove water column, affecting the new production in the ecosystems where they abound. Other metabolic pathways must be evaluated to further predict the role of sponges in these marine systems.