Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Introduced species wikipedia , lookup
Occupancy–abundance relationship wikipedia , lookup
Storage effect wikipedia , lookup
Ecological fitting wikipedia , lookup
Island restoration wikipedia , lookup
Fauna of Africa wikipedia , lookup
Habitat conservation wikipedia , lookup
Biodiversity action plan wikipedia , lookup
Environmental issues with coral reefs wikipedia , lookup
Theoretical ecology wikipedia , lookup
Latitudinal gradients in species diversity wikipedia , lookup
Journal of Animal Ecology 2005 74, 313–321 Trade-offs in resistance to competitors and predators, and their effects on the diversity of tropical marine sponges Blackwell Publishing, Ltd. JANIE L. WULFF Department of Biological Science, Florida State University, Tallahassee, FL 32306–1100, USA Summary 1. Consistently very high regional diversity of tropical marine sponges reflects a combination of high within-habitat diversity and distinctness of species composition among habitats. Distinctive sponge faunas of Caribbean coral reefs and mangroves seem to support the assumption that abiotic factors determine sponge diversity within habitats and faunal differences between habitats because these habitats differ greatly in abiotic characteristics and because lower species diversity on mangroves appears to reflect their inferiority as sponge habitat. 2. A way to test this assumption is provided by unusual mangrove cays in Belize that are inhabited by the typical Caribbean reef sponge fauna. Reciprocal transplant experiments, combined with caging (predator-free space) and artificial substrata (competitor-free space), demonstrated control of community membership by biological interactions for 12 common species: spongivorous predators excluded typical mangrove sponges from reef sponge assemblages, and reef sponges were excluded from mangrove sponge assemblages by competition. 3. Variation in growth rate was related inversely to variation in defences against predators in the species studied, suggesting a trade-off between resistance to competitors and to predators. 4. This trade-off influences community structure, as the key importance of competition for space among mangrove species results in lower within-habitat diversity, while multiple challenges, including predation, may maintain high diversity of reef sponges. Differences in species composition between habitats are maintained, as this trade-off precludes success of individual species as members of both faunas. 5. Most surprising is that typical faunas of mangroves and reefs are not tied to these habitats by abiotic factors. Greater sponge species diversity on the reef does not necessarily indicate superior conditions for sponges. Instead reefs may be a refuge for species that grow too slowly to coexist with typical mangrove species. Key-words: Caribbean, coral reefs, mangroves, Porifera, spongivory. Journal of Animal Ecology (2005) 74, 313–321 doi: 10.1111/j.1365-2656.2004.00925.x Introduction Intriguingly high regional diversity of tropical marine organisms has been attributed to competition, predation, mutualism, disturbance, recruitment patterns, geological age, physical habitat structure, areal extent of the region and various combinations of these. One consistent pattern among taxa and regions is that distinct species composition in each habitat (i.e. high betweenhabitat diversity) plays an especially important role in © 2005 British Ecological Society Correspondence: Janie L. Wulff, Department of Biological Science, Florida State University, Tallahassee, FL 32306 – 1100, USA. E-mail: [email protected] bolstering regional species counts in tropical seas (e.g. Knowlton & Jackson 1994; Ogden 1997; Paulay 1997). If species are sorted into habitats by how gracefully they cope with habitat-characteristic abiotic factors, the regional species pools for different habitats are functionally independent of each other. However, if biotic interactions influence species distributions across habitats, species could live in different habitats as distributions of their predators, competitors and mutualistic partners shift. A metacommunity viewpoint, acknowledging potential linkage of all species in the region, is then required. Thus as coral reefs and associated ecosystems slide more desperately into disrepair, knowing the relative importance of 314 J. L. Wulff © 2005 British Ecological Society, Journal of Animal Ecology, 74, 313–321 abiotic and biotic factors in sorting species into different habitats and maintaining within-habitat diversity of key groups is crucial (e.g. Bellwood & Hughes 2001). Sponges, like the much better-studied corals, fishes and shelled molluscs, are especially diverse and abundant, and are players of key functional roles in tropical marine systems (e.g. Paulay 1997; Diaz & Rützler 2001; Wulff 2001). However, sponges are set apart by intimidating identification and quantification challenges that have slowed studies of processes underlying their diversity patterns. Comprehensive faunal surveys of tropical sponges (e.g. Alcolado 1994; Zea 1994, 2001; Reed & Pomponi 1997; Hooper, Kennedy & Quinn 2002) demonstrate distinctive species compositions in different habitats. Abiotic factors have generally been held responsible for determining both habitat-distinctive species composition and within-habitat diversity. Universally acknowledged unusual chemistry of sponges has been invoked to explain apparent relative immunity to control by interactions (e.g. Kubanek et al. 2002 and references therein). Reports of sponges being outcompeted are rare (Sutherland 1980; Thacker et al. 1998), although sponges often outcompete neighbours of other taxa (e.g. Jackson & Buss 1975; Vicente 1990; Rützler & Muzik 1993; Aerts & van Soest 1997). Similarly, predators restrict some sponge species to refuges (e.g. Wulff 1988, 1995b, 1997b; Dunlap & Pawlik 1996, 1998), but the influence of predation on sponge diversity has barely been considered (Wulff 1994, 1997c; van Dam & Diez 1997). Caution in interpretation is advised by the possibility that biotic influences can be invisible if they curtail distributions so effectively that potentially competing species, or predator and prey species, rarely coexist. Experiments are required. Coral reefs and mangroves have distinct sponge faunas that contribute substantially to the region-wide Caribbean tally of over 640 described sponge species (van Soest 1994). An ideal situation for determining the relative importance of biological and abiotic factors for within-habitat diversity and habitat-distinctive sponge faunas of mangroves and coral reefs is provided by two sets of mangrove cays on the Belize Barrier Reef. The sponge fauna on mangrove roots at Twin Cays is typical of mangrove stands throughout the western Atlantic (Rützler et al. 2000; Wulff 2000, and references therein), but the sponge fauna on the Pelican Cays mangroves is unusual in that it is typical of shallow Caribbean coral reefs (Wulff 2000). The many abiotic differences that otherwise confound comparisons between mangroves and coral reefs (reefs generally have more light, less turbidity, fewer nutrients, more substratum continuity and more exposure to physical disturbance) are minimized, facilitating experimental evaluation of biological factors. The proximate focus of this study was to determine if biological interactions maintain the distinction between the typical sponge faunas of mangroves and coral reefs. Experiments tested two specific hypotheses: (1) sponge species typical of mangroves are consumed readily by spongivores and are therefore restricted to typical mangrove stands from which spongivores are absent and (2) sponge species typical of coral reefs are prevented from inhabiting typical mangroves by competition from mangrove sponge species, which grow more rapidly. I used the direct approach of reciprocal transplant experiments between the Pelican Cays and Twin Cays, augmented by cages (predator-free space) and artificial substrata (competitor-free space). Patterns of growth and survival of reciprocally transplanted sponges address the importance of biotic factors for sponge distribution and diversity on three levels, as follows. (1) Region: do competition and predation influence the striking distinction between the mangrove and coral-reef sponge faunas in the Caribbean? (2) Community: does within-habitat sponge diversity reflect the role of biological interactions in determining faunal membership? (3) Species: do trade-offs between resistance to competitors and resistance to predators preclude success of individual species as members of both faunas? Methods Twin Cays, a mangrove stand with a typical tropical western Atlantic mangrove sponge fauna, is a set of offshore cays built on peat banks, pervaded by channels and bays and surrounded by sediment and sea-grass meadows (Rützler et al. 2000; Wulff 2000, and references therein; maps in both papers). In the Pelican Cays, where a sponge fauna typical of shallow Caribbean coral reefs inhabits mangrove roots (Wulff 2000), the mangroves are embedded in peat banks on the tops of coral reefs. All but four of the 30 most common sponge species on the Pelican Cays mangroves are common inhabitants of shallow coral reefs (Wulff 2000). Prop roots at Twin Cays and the Pelican Cays together harbour a total of 167 sponge species and distinct forms, but 78% of those are found in only one of these two sets of cays, and many of the species that live in both are rare in one or the other (Rützler et al. 2000). The site chosen for experiments at Twin Cays, 3 km north-west of the Carrie Bow Cay research station of the Smithsonian Institution, is a channel known as Hidden Creek. In the Pelican Cays, 16 km south-west of Carrie Bow Cay, two sites were chosen: one at Manatee Cay, on the far side of the pond (200 m away) from the entrance, and the other at Cat Cay, to the left of and just 80 m inside the pond entrance. At Carrie Bow Cay, experiments were established among large corals on the shallow reef south-west of the island. Six of the most common sponge species at the Pelican Cays and six of the most common sponge species at Twin Cays were chosen for transplant experiments. All of these species had been accorded relative abundance 315 Growth-defence trade-offs and sponge diversity © 2005 British Ecological Society, Journal of Animal Ecology, 74, 313–321 ranks of ‘3’ (the highest) in their home cays in qualitative evaluations by a group of Caribbean sponge specialists (Rützler et al. 2000), and all were naturally absent or rare in the other set of cays. Species chosen from the Twin Cays community were Biemna caribea Pulitzer-Finali, Tedania ignis (Duch. & Mich.), Lissodendoryx isodictyalis (Carter) (all order Poecilosclerida), Amorphinopsis sp., Halichondria magniconulosa Hechtel (both order Halichondrida) and Haliclona implexiformis (Hechtel) (order Haplosclerida). All six species grow as clusters of volcano-shaped mounds. All except Amorphinopsis sp. are typical of mangrove roots throughout the Caribbean (Wulff 2000). Species chosen from the Pelican Cays community were Iotrochota birotulata (Higgin), Desmapsamma anchorata (Carter), Mycale laevis (Carter), Monanchora arbuscula (Duch. & Mich.) (all order Poecilosclerida), Amphimedon compressa Duch. & Mich. (order Haplosclerida) and Aplysina fulva (Pallas) (order Verongida). Four of these species have erect branching growth forms, while M. laevis and M. arbuscula form clusters of mounds from which branches sometimes extend. All six are among the most common species on shallow Caribbean coral reefs (see, e.g. Alvarez, Diaz & McLaughlin 1990; Alcolado 1994; Wulff 1994, 2000). Genotype was controlled in all experiments. From each individual, pieces (three for Twin Cays sponges, four for Pelican Cays sponges) were cut to similar size, shape and distribution of intact surface tissue. Cut pieces were kept in the field in small mesh baskets until cut edges healed. The volume of each sponge piece was measured by displacement of water in a graduated cylinder. Initial volumes ranged from 3 to 10 cm3, but most were 4 – 7 cm3. Sponges were transported in a large cooler that had been soaked in seawater, and the sponges were never exposed to air except for a second or two as their volumes were measured. Three prepared pieces of each of 13–16 individuals of each of the six species from Twin Cays (typical mangrove sponge fauna) were attached with beaded nylon cable ties 1 mm in diameter to (1) the original home root (control), (2) a root at Pelican Cays inside a small plastic cage (protected from predators) and (3) the same root at the Pelican Cays but outside the cage. The four prepared pieces of each of 12–15 individuals of each of the species from the Pelican Cays (typical shallow coral reef sponge fauna) were attached to (1) the original home root (control), (2) a root at Twin Cays, (3) a piece of presoaked pvc pipe (competitor-free space) suspended among the mangrove roots at Twin Cays and (4) a piece of clean coral rubble attached to a stainless steel stake inserted into the reef at Carrie Bow Cay at about 2·5 m depth (normal habitat for these reef species). Four pieces of the same size, shape and distribution of surface tissue were the maximum that could be cut from a single individual of most species, preventing perfect symmetry in the experimental design. However, preliminary experiments and observations had indicated that no clarity would be lost by not including cages at Twin Cays or pvc pipes in the Pelicans, and the fates of mangrove species transplanted to the reef from Twin Cays were followed in the predation experiments described below. Transplants were situated so that no other sponges or other sessile animals touched them. All 544 transplanted sponges were checked for reattachment and survival after 2–3 days. After 7 months (February 2002), a series of external measurements were used to estimate volumes by approximation to the volumes of appropriate conglomerations of geometric solids. To determine growth rates for reef sponges on reefs without confounding by storm-caused partial mortality, individuals of four of the reef sponge species were also grown on Guigalatupo reef, in the San Blas Islands, Panama, where hurricane damage is almost never a factor. Individuals of I. birotulata, A. compressa, A. fulva and D. anchorata were cut to initial sizes in the same range as those in the Belize experiments (most individuals 4–7 cm3), reattached to substrata on the reef, and re-measured after 7·6 months. To augment the caging experiments in the Pelican Cays, Twin Cays sponges were also brought to the Carrie Bow Cay reef, where greater site accessibility made detailed observations of fish feeding feasible. Another typical mangrove species from the order Haplosclerida, H. curaçaoensis (van Soest), was added to the experiments to balance taxonomic representation. Fish reacted differently to a blue–yellow morph and a purple morph of L. isodictyalis, so these were treated as distinct choices. For each of 12 feeding experiments (one per day), pieces of each of the eight species or colour morphs were cut to the same size, 6 cm3, and attached with small cable ties to coral rubble on stakes. Some sponge species concentrate defences in their surfaces (Uriz et al. 1996; Wulff 1997b; Schupp et al. 1999), so surfaces were allowed to heal before sponges were presented to fish. For each trial, the stakes were inserted into the reef so that the sponges appeared to be growing on pieces of coral rubble. All bites taken from the sponges in the first 30 min were recorded, in the order taken. The time at which each sponge piece was entirely consumed was recorded. The sponges were checked again after 1 h and 24 h. Results Only 3 days after transplantation to the Pelican Cays mangrove roots, 100% of uncaged individuals of four of the typical mangrove species had been consumed, leaving only 39% and 53% of the individuals of Amorphinopsis sp. and H. implexiformis, respectively. Some caged individuals were also lost, possibly because cages were attached too loosely. I observed grey angelfish, Pomacanthus arcuatus (Linnaeus), consuming uncaged 316 J. L. Wulff experimental sponges and attempting to nudge cages aside. Survival of controls at Twin Cays was 100%, so it is possible that the 20-km boat voyage also caused some mortality of transplanted sponges. Such losses would not differ between treatments, however, and the difference in survival between sponges inside and outside cages was striking (73% vs. 15·3%, significantly different by the G-test, P < 0·001). After 7 months, 35% (17/49) of the sponges that had been alive in cages after 3 days were still alive and had grown, a few of them large enough to fill the cages. None of the uncaged sponges survived. When the cages were removed, the sponges that had survived inside them were all consumed within 2 days. Survival of controls on home roots at Twin Cays was 42–100%, depending on the species (mean 67%; data in Fig. 1). Mangrove sponges transplanted from Twin Cays to the Carrie Bow reef did not attract wrasses and other generalists and scavengers that normally swarm to cut or broken sponges, because cut surfaces had been allowed to heal. Grey angelfish P. arcuatus and redband parrotfish Sparisoma aurofrenatum fed on the sponges. The angelfish spread their attention over all edible sponge species, taking only a few bites of a sponge and moving on to a different species. During observations of 506 bites in 130 bouts of uninterrupted feeding, angelfish always consumed fewer than eight bites of one species before switching, except for five bouts of feeding on T. ignis or B. caribea, which continued for from 12 to 31 bites. These species were the first to be consumed entirely in every trial. The parrotfish always consumed H. magniconulosa first, and then turned to Amorphinopsis sp. They chased away fish attempting to feed on these species and fed on a single sponge until it was gone or they were chased away. All sponges of six of the seven species were eliminated from the reef by predation within 24 h, but the species varied in how readily they were consumed. Consistent preferences by the fish throughout the 12 days of the experiments divided the sponge species into four groups: (1) T. ignis and B. caribea were always consumed within 10 min; (2) H. magniconulosa, Amorphinopsis sp. and the blue colour morph of L. isodictyalis were consumed within 10 min in 50%, 30% and 18% of the trials, respectively, and always within the first hour; (3) purple L. isodictyalis and H. curaçaoensis were never entirely consumed within the first hour but always within 24 h; and (4) H. implexiformis was never consumed within 24 h. Surfaces of H. implexiformis individuals became colonized by diatoms and they disappeared within 3 days, for unknown reasons. © 2005 British Ecological Society, Journal of Animal Ecology, 74, 313–321 Fig. 1. (a) Survival of sponges from the Pelican Cays 7 months after transplantation to mangrove roots or pvc pipes in Twin Cays. (b) Mean specific growth (± 1 SE) after 7 months of sponges transplanted from the Pelican Cays to roots or pvc pipes at Twin Cays. Individuals with net size decrease were excluded. Species abbreviated as: Iotr birot, Iotrochota birotulata; Amph comp, Amphimedon compressa; Apl fulva, Aplysina fulva; Desm anch, Desmapsamma anchorata; Myc laevis, Mycale laevis; Mon arbusc, Monanchora arbuscula. Two of the species (D. anchorata and M. arbuscula) were traumatized by the 20-km boat ride from the Pelicans to Twin Cays and no individuals increased in size, so they were not included in the analysis. The other four species tolerated the boat ride well, as illustrated by similar survival without net decrease of controls on home roots in the Pelicans and transplants to pvc pipes at Twin Cays (53·5% vs. 50·8%, not significantly different by the G-test, P = 0·5). By 7 months, many of the initially successful reef sponge transplants on roots at Twin Cays were reduced to very tiny pieces with virtually no survival potential, so comparisons between treatments were confined to individuals that had not decreased in size. Survival without net decrease was significantly greater on pvc pipes than on roots (overall 50·8% vs. 25%, G-test, P < 0·001; for individual species, differences were significant by the G-test for I. birotulata and A. fulva, P < 0·025; and M. laevis, P < 0·05; Fig. 1a). Specific net growth (standardized by initial volume) of typical reef species transplanted from Pelican Cays to Twin Cays reflected heavy partial mortality. To minimize confounding of growth potential with partial mortality, individuals with net size decrease were not included in the analysis. Variances were high (Fig. 1b) and both members survived in too few genotype pairs 317 Growth-defence trade-offs and sponge diversity Fig. 2. Mean specific growth (± 1 SE) of sponge species typical of shallow Caribbean coral reefs on mangroves in Belize (open bars) and on a shallow coral reef in San Blas, Panama (stippled bars). Species names are abbreviated as in Fig. 1. Sample sizes on mangroves and reef, respectively, Iotr birot 7, 25; Amph compressa 9, 15; Aply fulva 7, 22; Desm anch 7, 8. Differences are significant by Welch’s approximate t-test for cases in which variances are different at P < 0·05 for all species except Desmapsamma anchorata. to allow the planned paired statistical testing. Net growth was greater on pvc than on mangrove roots for Pelican Cays sponges at Twin Cays for all four of the species (I. birotulata, A. compressa, A. fulva and M. laevis) for which the comparison could be made (Fig. 1b), but not significantly so (by Welch’s approximate t-tests for cases in which variances are unequal). The cause of mortality and partial mortality of reef-sponge species from Pelican Cays on Twin Cays roots was clear, as mangrove sponges had grown over the transplanted reef sponges. At the time of monitoring, 52% (14/27) of surviving Pelican Cays sponges on roots were being overgrown. Guided by labelled cable ties remaining on the roots, the recent demise by overgrowth of nine additional Pelican Cays sponges was discovered by excavating within neighbouring mangrove sponges. Mangrove species that overgrew experimental reef sponges were (in order of decreasing frequency) T. ignis, B. caribea, H. magniconulosa, H. curaçaoensis, Spongia tubulifera, and L. isodictyalis. Overgrowth was not preceded by tissue death. © 2005 British Ecological Society, Journal of Animal Ecology, 74, 313–321 Typical reef species transplanted from the Pelican Cays mangroves to the Carrie Bow Cay reef survived poorly, reflecting passage of a hurricane in the autumn of 2001. Although some portion of 39% of the individuals was still alive, 87% of them had decreased in size, many so drastically that they were smaller than 1 cm3. Confining the analysis to the four species that tolerated the boat ride well, overall survival with size increase of reef species on the Carrie Bow Reef was only 19·8% after 7 months, contrasting with the 53·5% of control indi- Fig. 3. Mean specific growth (± 1 SE) of control individuals of six sponge species typical of shallow coral reefs (dark bars) and six species typical of mangrove roots (open bars indicate rapid consumption by fish, stippled bars indicate moderate consumption). Reef species abreviated as in Fig. 1; mangrove species as: Ted ignis, Tedania ignis; Biem car, Biemna caribea; Halich magn, Halichondria magniconulosa; Amorph sp., Amorphinopsis sp.; Liss isod, L. isodictyalis; Halicl imp, Haliclona implexiformis. viduals that increased in size on their home roots in the Pelican Cays (significantly different by the G-test, P < 0·001). Three of the species inhabiting both Pelican Cays mangroves and a shallow reef in Panama (I. birotulata, A. compressa, A. fulva) had significantly higher specific growth rates on mangrove roots than on the reef (Fig. 2; Welch’s approximate t-test for cases in which variances are unequal, P < 0·05 in all three comparisons). D. anchorata grew much faster than the others and at nearly the same rate in the two habitats. Growth rates vary widely among the 12 species (data from controls avoid confounding of growth with partial mortality; Fig. 3). All of the reef species except D. anchorata (an unusually fast-growing species, Aerts & van Soest 1997; Wulff, in preparation) grew relatively slowly. The mangrove species fall into two groups: the very fast-growing species, T. ignis, H. magniconulosa and B. caribea and a group with intermediate growth rates. Mangrove and coral-reef species also varied widely in survival in their home mangrove cays. Survival and mean specific growth rate of control individuals (Fig. 4) are not related for the reef species (Kendall’s coefficient of rank correlation, P >> 0·1), but have a significant positive relationship for the mangrove species (P = 0·05). Discussion Distinct sponge faunas on mangrove roots in the Pelican Cays and Twin Cays are maintained by predation 318 J. L. Wulff Fig. 4. Specific growth and survival after 7 months for six species of common, typical reef sponges grown on their home roots in the Pelican Cays and six species of common, typical mangrove sponges grown on their home roots in Twin Cays. Growth and survival were positively correlated (Kendall’s coefficient of rank correlation; P = 0·05) for mangrove sponges, but not for reef sponges. © 2005 British Ecological Society, Journal of Animal Ecology, 74, 313–321 and competition, at least for six of the most common species from each set of cays. Uncaged mangrove sponges were eliminated quickly by predators in the Pelican Cays mangroves. Elimination of reef sponges from the Pelican Cays by competition with quickly growing typical mangrove species on Twin Cays mangrove roots was still in progress after 7 months, but many individuals had already succumbed. Experiments on the Carrie Bow reef confirm that predators can prevent common mangrove species from living on the reef. Sponge-feeding fishes fed as in previous reports of natural feeding in the field. Angelfish departed from their usual ‘smorgasbord’ feeding (i.e. continuously moving among sponge species) (Randall & Hartman 1968; Wulff 1994) only for the two species they consumed most readily. Parrotfish consumed a sponge until it was gone or they were chased away, exactly as they feed on exposed cryptic reef sponges (Wulff 1988, 1997b, 1997c). This is not the first report of reef fishes eating mangrove sponges. Gut contents of parrotfish feeding in mangroves contained spicules from one mangrove species (Dunlap & Pawlik 1998), and videos of reef fishes feeding on chunks of mangrove sponges on exposed racks showed consumption of four species (Dunlap & Pawlik 1996), but details of normal feeding behaviour were lost in feeding melees resulting from sudden appearances of large pieces of freshly cut sponges. If spongivores can inhabit Pelican Cays mangroves and prevent typical mangrove species from living there, why are these fishes absent from Twin Cays and other typical Caribbean mangrove stands? Three-dimensional structure of the reefs in which Pelican Cays mangroves are embedded may offer fishes hiding places that are not available in or near typical mangrove stands (Wulff 2000 and additional personal observation). Barracudas are not absent from mangroves. Competition among sessile organisms takes longer to demonstrate than predation, especially when competition is mediated by relative growth rates. Finding typical reef sponge transplants engulfed entirely by mangrove sponges that were not touching them when the experiments were established, while individuals of the same genotypes and initial sizes were thriving on pvc pipes less than 0·5 m away, left no doubt that overgrowth was eliminating reef sponges from Twin Cays mangroves. Elimination by overgrowth is unusual for sponges. There are three reports: adult sponges overgrowing recent recruits (Reiswig 1973), T. ignis overgrowing other sponges on settling plates (Sutherland 1980), and a specific pairwise interaction between an overgrowing species and an overgrown species (Thacker et al. 1998). However, most reports on interactions of sponges with other sponges have suggested or demonstrated mutual benefit (Rützler 1970; Sará 1970; Wulff 1997a; Wilcox, Hill & DeMeo 2002). Competitive superiority of mangrove sponges over transplanted reef sponges appears to be mediated by growth, as there was no evidence of chemical warfare. The three mangrove species that smothered neighbouring reef sponge transplants most frequently were also the three with the fastest growth rates (Fig. 3). The positive correlation between growth and survival of mangrove species (Fig. 4) links growth rate to success in this habitat, suggesting that competition among the mangrove species is also mediated by relative growth rates. The sole reef species with rapid growth was D. anchorata, a uniquely weedy species (Wulff, in preparation). Lack of a relationship between growth and survival of the reef sponge species may reflect the variety of challenges they face, including consumption by fish and starfish, smothering by sediments and breakage by physical disturbance (e.g. Wulff 1997a). In such a context, directing resources to concerns other than rapid growth may make sense. The passage of a hurricane was reflected in lower survival of Pelican Cay sponges on the reef, but abiotic conditions definitely did not inhibit sponges transplanted between mangrove cays, as Twin Cays sponges thrived inside cages (predator-free) in the Pelicans, and Pelican Cays sponges thrived on pvc pipes (competitorfree) at Twin Cays. Restriction of species to refuges implies that a ‘refuge’ is a less desirable place to live. Cryptic spaces in the reef frame (Wulff 1988, 1997c) or under rubble (Dunlap & Pawlik 1996) can constrain the size a sponge achieves, and referring to these as refuges may be reasonable for some species. Mangrove roots have also been considered refuges from predators (e.g. by Dunlap & Pawlik 1996; Wulff 2000) for mangrove sponge species, although additional experiments are required to determine if 319 Growth-defence trade-offs and sponge diversity mangrove sponges would grow and survive better in other habitats if spongivores were eliminated. Facultative mutualism with mangroves may also inhibit habitat switches of some mangrove species (Ellison, Farnsworth & Twilley 1996). Data in this report do demonstrate, however, that sponge species that typically inhabit reefs can grow and survive substantially better on mangrove roots than on the reef (Fig. 2). However, the more rapid growth of reef sponges on mangrove roots is insufficient to prevent overgrowth by still more rapidly growing mangrove species (Fig. 3). Rather than providing the ideal set of abiotic factors for coral reef sponge species, the reef may be a refuge for sponge species that grow too slowly to survive among members of the mangrove fauna. - © 2005 British Ecological Society, Journal of Animal Ecology, 74, 313–321 A trade-off between growth rate and defence is suggested by the faster growth and more frequent participation in overgrowth of the three mangrove species that were consumed most quickly by fishes; intermediate growth rates of less eagerly consumed mangrove species; and slow growth of the well-defended reef species (except the unusual D. anchorata). Data on consumption of the typical reef species were not collected in this study because it takes years to accumulate sufficient observations of natural feeding on well-defended sponges, but a hint of an inverse relationship between growth and defence is seen in data from a 12-year study of unmanipulated angelfish feeding on a completely censused sponge community. For the relatively quickly growing (Fig. 3) I. birotulata the ratio of number of bites taken to total volume of sponge tissue was 0·07 (426 bites : 6001·3 cm3), while these ratios for the more slowly growing A. fulva and A. compressa were only 0·02 (72 bites : 3626·3 cm3) and 0·01 (117 bites : 9767·3 cm3), respectively (data from Wulff 1994 and unpublished). Trade-offs between growth and defence are well studied for terrestrial plants (e.g. Messina et al. 2002 and references therein), but directly relevant data are rare for clonal marine animals. The one direct study of resource allocation in sponges (Becerro, Turon & Uriz 1995; Uriz et al. 1995) demonstrated shifts by the encrusting Mediterranean sponge Crambe crambe to greater investment in defensive and supportive structures, at the expense of somatic growth and reproduction, in environments where competition was important. Another study (Hill 1998) has suggested that angelfishes preferentially consume a sponge, Chondrilla nucula, that may grow quickly; but angelfish preference was assumed on the basis of gut content data (Randall & Hartman 1968) which were not corrected for relative availability of sponge species. This sponge might overgrow corals if not consumed (Vicente 1990; Hill 1998), so confirmation of fast growth and of angelfish preference for this species would be especially interesting. Negative associations of growth rate with defences can be interpreted in a variety of ways (see, e.g. Simms 1992) and are complicated by trade-offs among other aspects of living (see, e.g. Mauricio 1998). Although comparisons among species are confounded further by differences in skeletal materials, modes of reproduction and chemistry, and our virtually complete ignorance about how costly all these aspects of living actually are, they can offer insight into influence of trade-offs on community structure and function. : - Sponges are like most other taxa in exhibiting very high diversity in shallow tropical marine systems (e.g. Paulay 1997). Van Soest (1994) estimated that 640 described sponge species inhabit the tropical western Atlantic, and many more await description. Sponges are dominant space-occupying organisms on reefs (e.g. Diaz & Rützler 2001) and mangrove roots throughout the region (e.g. Sutherland 1980; Ellison et al. 1996; Rützler et al. 2000; Wulff 2000). The key functional roles played by sponges in these systems are not covered by other organisms (Diaz & Rützler 2001; Wulff 2000). Understanding the relative importance of biotic and abiotic factors in maintaining sponge diversity has become crucial as conservation becomes more pressing. Distinctiveness of sponge faunas in different habitats has been attributed to abiotic factors, with which sponge distributions are often well correlated (see, e.g.Wilkinson & Evans 1989; Diaz et al. 1990; Alcolado 1994; Zea 1994). However, although abiotic differences between coral reefs and mangroves are many and well correlated with differences in the sponge faunas, in this first experimental test the causal relationship between abiotic factors and habitat distributions of sponge species is shown to be secondary. Within-habitat sponge diversity has also been attributed to abiotic factors. Negative influences have been attributed to physical disturbance, sunlight and sedimentation (see, e.g. Wilkinson & Evans 1989; Alvarez et al. 1990; Zea 2001 and references therein). Positive influences have been attributed to high substratum area, low turbidity, and close proximity of propagule source habitats (Rützler et al. 2000). It is probable that all of these factors could influence sponge diversity, but the contrasting systems in this study, with 2·5-fold differences in species diversity (57 species at Twin Cays and 147 species in the Pelican Cays were reported by Rützler et al. 2000), and in which competition or predation strongly influence membership, suggest a look at how interactions might also influence within-habitat diversity. In systems in which effectiveness at gaining space is key to survival of sessile organisms, competitively dominant species may overwhelm all others, lowering diversity. This expectation must be modified for systems characterized by discontinuous habitat structure. 320 J. L. Wulff © 2005 British Ecological Society, Journal of Animal Ecology, 74, 313–321 Sutherland (1980) pointed out that the discontinuous substrata provided by mangrove roots can increase diversity by preventing space monopolization by competitive dominants across large continuous areas, a key insight that has subsequently aided understanding of many other systems. The outcome for the typical mangrove root community is that diversity may be lowered on a particular root as fast-growing species overwhelm others, but discontinuous substrata slow elimination from the system, resulting in moderate overall species diversity. In contrast, in the Pelican Cays, where typical reefsponge species live on mangrove roots, spongivores may prevent community domination by faster-growing sponge species. This mechanism for maintaining high diversity of sessile organisms was pointed out early on by studies of preferential consumption of competitive dominants by rabbits and starfish (Tansley & Adamson 1925; Paine 1966). If an inverse relationship between growth rate and defences holds for more species than the 12 most abundant ones chosen for these experiments, predators are at least partly responsible for the exceptionally high sponge diversity of the typical shallow coral reef sponge fauna. This is the opposite conclusion from previous studies (Dunlap & Pawlik 1996, 1998) which suggested that spongivores decrease reef sponge diversity by excluding mangrove species. The ability of mangrove sponge species to outcompete reef species, demonstrated first in the present study, was the missing link between spongivory and very high diversity on reefs. Substantially poorer survival of sponges transplanted from the Pelican Cays to the Carrie Bow reef supports assertions that abiotic factors can serve as filters, excluding some species from a habitat (e.g. Wilkinson & Evans 1989; Alvarez et al. 1990; Alcolado 1994). However, for species not inhibited by such filters, ecological interactions affect sponge diversity on three scales, as follows. (1) Region: competition and predation strongly influence the between-habitat diversity of Caribbean mangrove and coral reef sponge faunas. (2) Community: control of mangrove-fauna membership by competition lowers species diversity, whereas a variety of controls on reef-fauna membership, including predation, may increase the number of species that coexist on reefs. (3) Species: the trade-off between growth (resistance to competitors) and resistance to predators precludes success of individual species as members of both faunas. Surprisingly, although members of the typical coral reef sponge fauna and the typical mangrove root sponge fauna appear unable to intermix, and thus remain distinct sets of species, these faunas are not actually tied to the habitats in which they are found normally. The persistent distinction between these two faunas is not determined by habitat-characteristic abiotic factors, but is a community-level reflection of the trade-off between growth and defences against predators. In our ‘high diversity is good’ context of evaluating ecological systems, the higher species diversity on coral reefs than on mangroves has implied that the coral reef is the superior habitat for tropical sponges. In fact, the higher diversity may reflect the multiple challenges that make living on a coral reef more of a struggle for sponges. Mangroves, with higher nutrients, lower physical disturbance and no predators, offer typical reef sponges better survival and growth, but trade-offs between defences and growth put this paradise out of reach as long as it is inhabited by typical mangrove species that have traded the ability to cope with challenges for the ability to grow more rapidly. Acknowledgements Fieldwork for this project was supported by the National Museum of Natural History’s Caribbean Coral Reef Ecosystems Program (CCRE Contribution no. 693). I am grateful for the vigorous discussion and comradeship of fellow participants in the International Sponge Systematics Workshop convened at Carrie Bow Cay in 1997. Thoughtful comments from J. Travis, N. Underwood, D. Ferrell, T. Swain and anonymous reviewers greatly improved the manuscript. References Aerts, L.A.M. & van Soest, R.W.M. (1997) Quantification of sponge /coral interactions in a physically stressed reef community, NE Colombia. Marine Ecology Progress Series, 148, 125 – 134. Alcolado, P.M. (1994) General trends in coral reefs sponge communities in Cuba. Sponges in Time and Space: Biology, Chemistry, Paleontology (eds R.W.M. van Soest, T.M.G. van Kempen & J.-C.A.A. Braekman), pp. 251 – 256. A. A. Balkema, Rotterdam. Alvarez, B., Diaz, M.C. & Laughlin, R.A. (1990) The sponge fauna on a fringing coral reef in Venezuela, I. Composition, distribution, and abundance. New Perspectives in Sponge Biology (ed. K. Rützler), pp. 358 – 366. Smithsonian Institution Press, Washington DC. Becerro, M.A., Turon, X. & Uriz, M.J. (1995) Natural variation of toxicity in encrusting sponge Crambe crambe (Schmidt) in relation to size and environment. Journal of Chemical Ecology, 21, 1931 – 1946. Bellwood, D.R. & Hughes, T.P. (2001) Regional-scale assembly rules and biodiversity of coral reefs. Science, 292, 1532 –1534. van Dam, R.P. & Diez, C.E. (1997) Predation by hawksbill turtles at Mona Island, Puerto Rico. Proceedings of the 8th International Coral Reef Symposium, Panama, 2, 1421– 1426. Diaz, C., Alvarez, B. & Laughlin, R.A. (1990) The sponge fauna on a fringing reef in Venezuela, II. Community structure. New Perspectives in Sponge Biology (ed. K. Rützler), pp. 367 – 375. Smithsonian Institution Press, Washington, DC. Diaz, C. & Rützler, K. (2001) Sponges: an essential component of Caribbean coral reefs. Bulletin of Marine Science, 69, 535 – 546. Dunlap, M. & Pawlik, J.R. (1996) Video-monitored predation by Caribbean reef fishes on an array of mangrove and reef sponges. Marine Biology, 126, 117 – 123. Dunlap, M. & Pawlik, J.R. (1998) Spongivory by parrotfish in Florida mangrove and reef habitats. PSZN: Marine Ecology, 19, 325 – 337. 321 Growth-defence trade-offs and sponge diversity © 2005 British Ecological Society, Journal of Animal Ecology, 74, 313–321 Ellison, A.M., Farnsworth, E.J. & Twilley, R.R. (1996) Facultative mutualism between red mangroves and rootfouling sponges in Belizean mangal. Ecology, 77, 2431 – 2444. Hill, M.S. (1998) Spongivory on Caribbean reefs releases corals from competition with sponges. Oecologia, 117, 143 – 150. Hooper, J.N.A., Kennedy, J.A. & Quinn, R.J. (2002) Biodiversity ‘hotspots’. Patterns of richness and endemism, and taxonomic affinities of tropical Australian sponges (Porifera). Biodiversity Conservation, 11, 851 – 885. Jackson, J.B.C. & Buss, L.W. (1975) Allelopathy and spatial competition among coral reef invertebrates. Proceedings of the National Academy of Science USA, 72, 5160 – 5163. Knowlton, N. & Jackson, J.B.C. (1994) New taxonomy and niche partitioning on coral reefs: jack of all trades or master of some? Trends in Ecology and Evolution, 9, 7 – 9. Kubanek, J., Whalen, K.E., Engel, S., Kelly, S.R., Henkel, T.P., Fenical, W. & Pawlik, J.R. (2002) Multiple defensive roles for triterpene glycosides from two Caribbean sponges. Oecologia, 131, 125 – 136. Mauricio, R. (1998) Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. American Naturalist, 151, 20 – 28. Messina, F.J., Durham, S.L., Richards, J.H. & McArthur, E.D. (2002) Trade-off between plant growth and defense? A comparison of sagebrush populations. Oecologia, 131, 43 – 51. Ogden, J.C. (1997) Ecosystem interactions in the tropical coastal seascape. Life and Death of Coral Reefs (ed. C. Birkeland), pp. 288 – 297. Chapman & Hall, New York. Paine, R.T. (1966) Food web complexity and species diversity. American Naturalist, 100, 65 – 75. Paulay, G. (1997) Diversity and distribution of reef organisms. Life and Death of Coral Reefs (ed. C. Birkeland), pp. 298 – 353. Chapman & Hall, New York. Randall, J.E. & Hartman, W.D. (1968) Sponge-feeding fishes of the West Indies. Marine Biology, 1, 216 – 225. Reed, J.K. & Pomponi, S.A. (1997) Biodiversity and distribution of deep and shallow water sponges in the Bahamas. Proceedings of the 8th International Coral Reef Symposium, Panama, 2, 1387 – 1392. Reiswig, H.M. (1973) Population dynamics of three Jamaican Demospongiae. Bulletin of Marine Science., 23, 191 – 226. Rützler, K. (1970) Spatial competition among Porifera: solution by epizoism. Oecologia, 5, 85 – 95. Rützler, K., Diaz, M.C., van Soest, R.W.M., Zea, S., Smith, K.P., Alvarez, B. & Wulff, J.L. (2000) Diversity of sponge fauna in mangrove ponds, Pelican Cays, Belize. Atoll Research Bulletin, 477, 231 – 250. Rützler, K. & Muzik, K. (1993) Terpios hoshinota, a new cyanobacteriosponge threatening Pacific reefs. Scientia Marina, 57, 395 – 403. Sará, M. (1970) Competition and cooperation in sponge populations. Symposium of the Zoological Society of London, 25, 273 – 284. Schupp, P., Eder, C., Paul, V. & Proksch, P. (1999) Distribution of secondary metabolites in the sponge Oceanapia sp. and its ecological implications. Marine Biology, 135, 573 – 580. Simms, E.L. (1992) Costs of plant resistance to herbivory. Plant Resistance to Herbivores and Pathogens (eds R.S. Fritz & E.L. Simms), pp. 392 – 425. University of Chicago Press, Chicago. van Soest, R.W.M., (1994) Demosponge distribution patterns. Sponges in Time and Space: Biology, Chemistry, Paleontology (eds R.W.M. van Soest, T.M.G. van Kempen, & J.-C. Braekman), pp. 213–224. A. A. Balkema, Rotterdam. Sutherland, J.P. (1980) Dynamics of the epibenthic community on roots of the mangrove Rhizophora mangle, at Bahia de Buche, Venezuela. Marine Biology, 58, 75–84. Tansley, A.G. & Adamson, R.S. (1925) Studies of the vegetation of the English chalk. III. The chalk grasslands of the Hampshire–Sussex border. Journal of Ecology, 13, 177– 223. Thacker, R.W., Becerro, M.A., Lumbang, W.A. & Paul, V.J. (1998) Allelopathic interactions between sponges of a tropical reef. Ecology, 79, 1740 –1750. Uriz, M.J., Becerro, M.A., Tur, J.M. & Turon, X. (1996) Location of toxicity within the Mediterranean sponge Crambe crambe (Demospongiae: Poecilosclerida). Marine Biology, 124, 583 –590. Uriz, M.J., Turon, X., Becerro, M.A., Galera, J. & Lozano, J. (1995) Patterns of resource allocation to somatic, defensive, and reproductive functions in the Mediterranean encrusting sponge Crambe crambe (Demospongiae, Poecilosclerida). Marine Ecology Progress Series, 124, 159 – 170. Vicente, V. (1990) Overgrowth activity by the encrusting sponge Chondrilla nucula on a coral reef in Puerto Rico. New Perspectives in Sponge Biology (ed. K. Rützler), pp. 436– 442. Smithsonian Institution Press, Washington, DC. Wilcox, T.P., Hill, M. & DeMeo, K. (2002) Observations on a new two-sponge symbiosis from the Florida Keys. Coral Reefs, 21, 198 – 204. Wilkinson, C.R. & Evans, E. (1989) Sponge distribution across Davies Reef, Great Barrier Reef, relative to location, depth, and water movement. Coral Reefs, 8, 1–7. Wulff, J.L. (1988) Fish predation on cryptic sponges of Caribbean coral reefs. American Zoologist, 28, A166. Wulff, J.L. (1994) Sponge-feeding by Caribbean angelfishes, trunkfishes, and filefishes. Sponges in Time and Space: Biology, Chemistry, Paleontology (eds R.W.M. van Soest, T.M.G. van Kempen & J.-C. Braekman), pp. 265–271. A. A. Balkema, Rotterdam. Wulff, J.L. (1995b) Sponge-feeding by the Caribbean starfish Oreaster reticulatus. Marine Biology, 123, 313–325. Wulff, J.L. (1997a) Mutualisms among species of coral reef sponges. Ecology, 78, 146 – 159. Wulff, J.L. (1997b) Parrotfish predation on cryptic sponges of Caribbean coral reefs. Marine Biology, 129, 41–52. Wulff, J.L. (1997c) Causes and consequences of differences in sponge diversity and abundance between the Caribbean and eastern Pacific at Panama. Proceedings of the 8th International Coral Reef Symposium, Panama, 2, 377–1382. Wulff, J.L. (2000) Sponge predators may determine differences in sponge fauna between two sets of mangrove cays, Belize Barrier Reef. Atoll Research Bulletin, 477, 251– 263. Wulff, J.L. (2001) Assessing and monitoring coral reef sponges: why and how? Bulletin of Marine Science, 69, 831 – 846. Zea, S. (1994) Patterns of sponge and coral abundance in stressed coral reefs at Santa Marta, Colombian Caribbean. Sponges in Time and Space: Biology, Chemistry, Paleontology (eds R.W.M. van Soest, T.M.G. van Kempen & J.-C. Braekman), pp. 257 – 264. A. A. Balkema, Rotterdam. Zea, S. (2001) Patterns of sponge (Porifera, Demospongiae) distribution in remote, oceanic reef complexes of the southwestern Caribbean. Revista de la Acadamia Colombiana de Ciencias Exactas, Fisicas Y Naturales, 25, 579–592. Received 28 January 2004; accepted 13 August 2004