Journal of Animal Blackwell Publishing, Ltd. Ecology 2005 Trade-offs in resistance to competitors and predators, and 74, 313–321 their effects on the diversity of tropical marine sponges
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 com- bination 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 assem- blages by competition. 3. Variation in growth rate was related inversely to variation in defences against pred- ators 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 neces- sarily 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
bolstering regional species counts in tropical seas (e.g. Introduction Knowlton & Jackson 1994; Ogden 1997; Paulay 1997). Intriguingly high regional diversity of tropical marine If species are sorted into habitats by how gracefully organisms has been attributed to competition, predation, they cope with habitat-characteristic abiotic factors, mutualism, disturbance, recruitment patterns, geolog- the regional species pools for different habitats are ical age, physical habitat structure, areal extent of the functionally independent of each other. However, if region and various combinations of these. One consist- biotic interactions influence species distributions ent pattern among taxa and regions is that distinct across habitats, species could live in different habitats species composition in each habitat (i.e. high between- as distributions of their predators, competitors and habitat diversity) plays an especially important role in mutualistic partners shift. A metacommunity view- point, acknowledging potential linkage of all species Correspondence: Janie L. Wulff, Department of Biological in the region, is then required. Thus as coral reefs © 2005 British Science, Florida State University, Tallahassee, FL 32306– and associated ecosystems slide more desperately Ecological Society 1100, USA. E-mail: [email protected] into disrepair, knowing the relative importance of
314 abiotic and biotic factors in sorting species into differ- by spongivores and are therefore restricted to typical J. L. Wulff ent habitats and maintaining within-habitat diversity mangrove stands from which spongivores are absent of key groups is crucial (e.g. Bellwood & Hughes 2001). and (2) sponge species typical of coral reefs are pre- Sponges, like the much better-studied corals, fishes vented from inhabiting typical mangroves by competi- and shelled molluscs, are especially diverse and abun- tion from mangrove sponge species, which grow more dant, and are players of key functional roles in tropical rapidly. I used the direct approach of reciprocal trans- marine systems (e.g. Paulay 1997; Diaz & Rützler 2001; plant experiments between the Pelican Cays and Twin Wulff 2001). However, sponges are set apart by inti- Cays, augmented by cages (predator-free space) and midating identification and quantification challenges artificial substrata (competitor-free space). that have slowed studies of processes underlying their Patterns of growth and survival of reciprocally trans- diversity patterns. Comprehensive faunal surveys of planted sponges address the importance of biotic fac- tropical sponges (e.g. Alcolado 1994; Zea 1994, 2001; tors for sponge distribution and diversity on three levels, Reed & Pomponi 1997; Hooper, Kennedy & Quinn as follows. (1) Region: do competition and predation 2002) demonstrate distinctive species compositions in influence the striking distinction between the mangrove different habitats. Abiotic factors have generally been and coral-reef sponge faunas in the Caribbean? (2) Com- held responsible for determining both habitat-distinctive munity: does within-habitat sponge diversity reflect the species composition and within-habitat diversity. role of biological interactions in determining faunal Universally acknowledged unusual chemistry of sponges membership? (3) Species: do trade-offs between resistance has been invoked to explain apparent relative immu- to competitors and resistance to predators preclude nity to control by interactions (e.g. Kubanek et al. 2002 success of individual species as members of both faunas? and references therein). Reports of sponges being outcompeted are rare (Sutherland 1980; Thacker et al. Methods 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. Twin Cays, a mangrove stand with a typical tropical Wulff 1988, 1995b, 1997b; Dunlap & Pawlik 1996, 1998), western Atlantic mangrove sponge fauna, is a set of off- but the influence of predation on sponge diversity has shore cays built on peat banks, pervaded by channels barely been considered (Wulff 1994, 1997c; van Dam & and bays and surrounded by sediment and sea-grass Diez 1997). meadows (Rützler et al. 2000; Wulff 2000, and references Caution in interpretation is advised by the possibil- therein; maps in both papers). In the Pelican Cays, ity that biotic influences can be invisible if they curtail where a sponge fauna typical of shallow Caribbean distributions so effectively that potentially competing coral reefs inhabits mangrove roots (Wulff 2000), the species, or predator and prey species, rarely coexist. mangroves are embedded in peat banks on the tops of Experiments are required. Coral reefs and mangroves coral reefs. All but four of the 30 most common sponge have distinct sponge faunas that contribute substan- species on the Pelican Cays mangroves are common tially to the region-wide Caribbean tally of over 640 inhabitants of shallow coral reefs (Wulff 2000). Prop described sponge species (van Soest 1994). An ideal situ- roots at Twin Cays and the Pelican Cays together ation for determining the relative importance of bio- harbour a total of 167 sponge species and distinct forms, logical and abiotic factors for within-habitat diversity but 78% of those are found in only one of these two sets and habitat-distinctive sponge faunas of mangroves of cays, and many of the species that live in both are and coral reefs is provided by two sets of mangrove cays rare in one or the other (Rützler et al. 2000). on the Belize Barrier Reef. The sponge fauna on man- The site chosen for experiments at Twin Cays, 3 km grove roots at Twin Cays is typical of mangrove stands north-west of the Carrie Bow Cay research station of throughout the western Atlantic (Rützler et al. 2000; the Smithsonian Institution, is a channel known as Wulff 2000, and references therein), but the sponge fauna Hidden Creek. In the Pelican Cays, 16 km south-west on the Pelican Cays mangroves is unusual in that it is of Carrie Bow Cay, two sites were chosen: one at Man- typical of shallow Caribbean coral reefs (Wulff 2000). atee Cay, on the far side of the pond (200 m away) from The many abiotic differences that otherwise confound the entrance, and the other at Cat Cay, to the left of and comparisons between mangroves and coral reefs (reefs just 80 m inside the pond entrance. At Carrie Bow Cay, generally have more light, less turbidity, fewer nutrients, experiments were established among large corals on more substratum continuity and more exposure to the shallow reef south-west of the island. physical disturbance) are minimized, facilitating experi- mental evaluation of biological factors. The proximate focus of this study was to determine if © 2005 British biological interactions maintain the distinction between Six of the most common sponge species at the Pelican Ecological Society, Journal of Animal the typical sponge faunas of mangroves and coral reefs. Cays and six of the most common sponge species at Ecology, 74, Experiments tested two specific hypotheses: (1) sponge Twin Cays were chosen for transplant experiments. All 313–321 species typical of mangroves are consumed readily of these species had been accorded relative abundance
315 ranks of ‘3’ (the highest) in their home cays in qualita- cages at Twin Cays or pvc pipes in the Pelicans, and the Growth-defence tive evaluations by a group of Caribbean sponge fates of mangrove species transplanted to the reef from trade-offs and specialists (Rützler et al. 2000), and all were naturally Twin Cays were followed in the predation experiments sponge diversity absent or rare in the other set of cays. described below. Species chosen from the Twin Cays community were Transplants were situated so that no other sponges Biemna caribea Pulitzer-Finali, Tedania ignis (Duch. & or other sessile animals touched them. All 544 trans- Mich.), Lissodendoryx isodictyalis (Carter) (all order planted sponges were checked for reattachment and Poecilosclerida), Amorphinopsis sp., Halichondria magni- survival after 2–3 days. After 7 months (February 2002), conulosa Hechtel (both order Halichondrida) and a series of external measurements were used to estimate Haliclona implexiformis (Hechtel) (order Haplosclerida). volumes by approximation to the volumes of appropriate All six species grow as clusters of volcano-shaped conglomerations of geometric solids. mounds. All except Amorphinopsis sp. are typical of To determine growth rates for reef sponges on reefs mangrove roots throughout the Caribbean (Wulff 2000). without confounding by storm-caused partial mortality, Species chosen from the Pelican Cays community were individuals of four of the reef sponge species were also Iotrochota birotulata (Higgin), Desmapsamma ancho- grown on Guigalatupo reef, in the San Blas Islands, rata (Carter), Mycale laevis (Carter), Monanchora Panama, where hurricane damage is almost never a arbuscula (Duch. & Mich.) (all order Poecilosclerida), factor. Individuals of I. birotulata, A. compressa, A. fulva Amphimedon compressa Duch. & Mich. (order Haplo- and D. anchorata were cut to initial sizes in the same sclerida) and Aplysina fulva (Pallas) (order Verongida). range as those in the Belize experiments (most indivi- Four of these species have erect branching growth duals 4–7 cm3), reattached to substrata on the reef, and forms, while M. laevis and M. arbuscula form clusters re-measured after 7·6 months. 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). To augment the caging experiments in the Pelican Cays, Genotype was controlled in all experiments. From Twin Cays sponges were also brought to the Carrie Bow each individual, pieces (three for Twin Cays sponges, Cay reef, where greater site accessibility made detailed four for Pelican Cays sponges) were cut to similar size, observations of fish feeding feasible. Another typical shape and distribution of intact surface tissue. Cut mangrove species from the order Haplosclerida, H. pieces were kept in the field in small mesh baskets until curaçaoensis (van Soest), was added to the experiments cut edges healed. The volume of each sponge piece was to balance taxonomic representation. Fish reacted dif- measured by displacement of water in a graduated ferently to a blue–yellow morph and a purple morph of cylinder. Initial volumes ranged from 3 to 10 cm3, but L. isodictyalis, so these were treated as distinct choices. most were 4–7 cm3. Sponges were transported in a For each of 12 feeding experiments (one per day), large cooler that had been soaked in seawater, and the pieces of each of the eight species or colour morphs were sponges were never exposed to air except for a second cut to the same size, 6 cm3, and attached with small or two as their volumes were measured. cable ties to coral rubble on stakes. Some sponge species Three prepared pieces of each of 13–16 individuals concentrate defences in their surfaces (Uriz et al. 1996; of each of the six species from Twin Cays (typical man- Wulff 1997b; Schupp et al. 1999), so surfaces were allowed grove sponge fauna) were attached with beaded nylon to heal before sponges were presented to fish. For each cable ties 1 mm in diameter to (1) the original home trial, the stakes were inserted into the reef so that the root (control), (2) a root at Pelican Cays inside a small sponges appeared to be growing on pieces of coral rub- plastic cage (protected from predators) and (3) the ble. All bites taken from the sponges in the first 30 min same root at the Pelican Cays but outside the cage. The were recorded, in the order taken. The time at which four prepared pieces of each of 12–15 individuals of each sponge piece was entirely consumed was recorded. each of the species from the Pelican Cays (typical shal- The sponges were checked again after 1 h and 24 h. low coral reef sponge fauna) were attached to (1) the original home root (control), (2) a root at Twin Cays, Results (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 Only 3 days after transplantation to the Pelican Cays Cay at about 2·5 m depth (normal habitat for these reef mangrove roots, 100% of uncaged individuals of four species). Four pieces of the same size, shape and distri- of the typical mangrove species had been consumed, bution of surface tissue were the maximum that could leaving only 39% and 53% of the individuals of Amor- © 2005 British be cut from a single individual of most species, prevent- phinopsis sp. and H. implexiformis, respectively. Some Ecological Society, Journal of Animal ing perfect symmetry in the experimental design. How- caged individuals were also lost, possibly because cages Ecology, 74, ever, preliminary experiments and observations had were attached too loosely. I observed grey angelfish, 313–321 indicated that no clarity would be lost by not including Pomacanthus arcuatus (Linnaeus), consuming uncaged
316 experimental sponges and attempting to nudge cages to heal. Grey angelfish P. arcuatus and redband parrot- J. L. Wulff aside. Survival of controls at Twin Cays was 100%, so it fish Sparisoma aurofrenatum fed on the sponges. The is possible that the 20-km boat voyage also caused angelfish spread their attention over all edible sponge some mortality of transplanted sponges. Such losses species, taking only a few bites of a sponge and moving would not differ between treatments, however, and the on to a different species. During observations of 506 difference in survival between sponges inside and outside bites in 130 bouts of uninterrupted feeding, angelfish cages was striking (73% vs. 15·3%, significantly different always consumed fewer than eight bites of one species by the G-test, P < 0·001). before switching, except for five bouts of feeding on T. After 7 months, 35% (17/49) of the sponges that had ignis or B. caribea, which continued for from 12 to 31 bites. been alive in cages after 3 days were still alive and had These species were the first to be consumed entirely in grown, a few of them large enough to fill the cages. None every trial. The parrotfish always consumed H. magni- of the uncaged sponges survived. When the cages were conulosa first, and then turned to Amorphinopsis sp. removed, the sponges that had survived inside them They chased away fish attempting to feed on these were all consumed within 2 days. Survival of controls species and fed on a single sponge until it was gone or on home roots at Twin Cays was 42–100%, depending they were chased away. on the species (mean 67%; data in Fig. 1). All sponges of six of the seven species were elimi- Mangrove sponges transplanted from Twin Cays to nated from the reef by predation within 24 h, but the the Carrie Bow reef did not attract wrasses and other species varied in how readily they were consumed. generalists and scavengers that normally swarm to cut or Consistent preferences by the fish throughout the broken sponges, because cut surfaces had been allowed 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, Amor- phinopsis 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 dis- appeared within 3 days, for unknown reasons.
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 differ- ent 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, differ- ences were significant by the G-test for I. birotulata and Fig. 1. (a) Survival of sponges from the Pelican Cays 7 months A. fulva, P < 0·025; and M. laevis, P < 0·05; Fig. 1a). after transplantation to mangrove roots or pvc pipes in Twin Specific net growth (standardized by initial volume) Cays. (b) Mean specific growth (± 1 SE) after 7 months of of typical reef species transplanted from Pelican Cays sponges transplanted from the Pelican Cays to roots or pvc to Twin Cays reflected heavy partial mortality. To © 2005 British pipes at Twin Cays. Individuals with net size decrease minimize confounding of growth potential with partial Ecological Society, were excluded. Species abbreviated as: Iotr birot, Iotrochota Journal of Animal birotulata; Amph comp, Amphimedon compressa; Apl fulva, mortality, individuals with net size decrease were not Ecology, 74, Aplysina fulva; Desm anch, Desmapsamma anchorata; Myc included in the analysis. Variances were high (Fig. 1b) 313–321 laevis, Mycale laevis; Mon arbusc, Monanchora arbuscula. 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 Fig. 3. Mean specific growth (± 1 SE) of control individuals Belize (open bars) and on a shallow coral reef in San Blas, of six sponge species typical of shallow coral reefs (dark bars) Panama (stippled bars). Species names are abbreviated as in and six species typical of mangrove roots (open bars indicate Fig. 1. Sample sizes on mangroves and reef, respectively, Iotr rapid consumption by fish, stippled bars indicate moderate birot 7, 25; Amph compressa 9, 15; Aply fulva 7, 22; Desm anch consumption). Reef species abreviated as in Fig. 1; mangrove 7, 8. Differences are significant by Welch’s approximate t-test species as: Ted ignis, Tedania ignis; Biem car, Biemna caribea; for cases in which variances are different at P < 0·05 for all Halich magn, Halichondria magniconulosa; Amorph sp., species except Desmapsamma anchorata. Amorphinopsis sp.; Liss isod, L. isodictyalis; Halicl imp, Haliclona implexiformis.
to allow the planned paired statistical testing. Net growth was greater on pvc than on mangrove roots viduals that increased in size on their home roots in the for Pelican Cays sponges at Twin Cays for all four of the Pelican Cays (significantly different by the G-test, species (I. birotulata, A. compressa, A. fulva and M. laevis) P < 0·001). for which the comparison could be made (Fig. 1b), but Three of the species inhabiting both Pelican Cays not significantly so (by Welch’s approximate t-tests for mangroves and a shallow reef in Panama (I. birotulata, cases in which variances are unequal). A. compressa, A. fulva) had significantly higher specific The cause of mortality and partial mortality of growth rates on mangrove roots than on the reef reef-sponge species from Pelican Cays on Twin Cays (Fig. 2; Welch’s approximate t-test for cases in which roots was clear, as mangrove sponges had grown over variances are unequal, P < 0·05 in all three compari- the transplanted reef sponges. At the time of monitor- sons). D. anchorata grew much faster than the others ing, 52% (14/27) of surviving Pelican Cays sponges on and at nearly the same rate in the two habitats. roots were being overgrown. Guided by labelled cable Growth rates vary widely among the 12 species (data ties remaining on the roots, the recent demise by over- from controls avoid confounding of growth with growth of nine additional Pelican Cays sponges was partial mortality; Fig. 3). All of the reef species except discovered by excavating within neighbouring mangrove D. anchorata (an unusually fast-growing species, Aerts sponges. Mangrove species that overgrew experimental & van Soest 1997; Wulff, in preparation) grew relatively reef sponges were (in order of decreasing frequency) slowly. The mangrove species fall into two groups: the T. ignis, B. caribea, H. magniconulosa, H. curaçaoensis, very fast-growing species, T. ignis, H. magniconulosa and Spongia tubulifera, and L. isodictyalis. Overgrowth was B. caribea and a group with intermediate growth rates. not preceded by tissue death. 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 Typical reef species transplanted from the Pelican Cays positive relationship for the mangrove species (P = 0·05). mangroves to the Carrie Bow Cay reef survived poorly, reflecting passage of a hurricane in the autumn of 2001. Discussion 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. Confin- © 2005 British ing the analysis to the four species that tolerated the Ecological Society, Journal of Animal boat ride well, overall survival with size increase of reef Ecology, 74, species on the Carrie Bow Reef was only 19·8% after Distinct sponge faunas on mangrove roots in the Peli- 313–321 7 months, contrasting with the 53·5% of control indi- can Cays and Twin Cays are maintained by predation 318 Competition among sessile organisms takes longer J. L. Wulff to demonstrate than predation, especially when com- petition 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 Fig. 4. Specific growth and survival after 7 months for six a specific pairwise interaction between an overgrowing species of common, typical reef sponges grown on their home species and an overgrown species (Thacker et al. 1998). roots in the Pelican Cays and six species of common, typical However, most reports on interactions of sponges with mangrove sponges grown on their home roots in Twin Cays. other sponges have suggested or demonstrated mutual Growth and survival were positively correlated (Kendall’s benefit (Rützler 1970; Sará 1970; Wulff 1997a; Wilcox, coefficient of rank correlation; P = 0·05) for mangrove sponges, but not for reef sponges. Hill & DeMeo 2002). Competitive superiority of man- grove sponges over transplanted reef sponges appears to be mediated by growth, as there was no evidence of chemical warfare. The three mangrove species that and competition, at least for six of the most common smothered neighbouring reef sponge transplants most species from each set of cays. Uncaged mangrove sponges frequently were also the three with the fastest growth were eliminated quickly by predators in the Pelican rates (Fig. 3). The positive correlation between growth and Cays mangroves. Elimination of reef sponges from the survival of mangrove species (Fig. 4) links growth rate Pelican Cays by competition with quickly growing to success in this habitat, suggesting that competition typical mangrove species on Twin Cays mangrove roots among the mangrove species is also mediated by relative was still in progress after 7 months, but many individuals growth rates. had already succumbed. The sole reef species with rapid growth was D. ancho- Experiments on the Carrie Bow reef confirm that rata, a uniquely weedy species (Wulff, in preparation). predators can prevent common mangrove species from Lack of a relationship between growth and survival living on the reef. Sponge-feeding fishes fed as in pre- of the reef sponge species may reflect the variety of vious reports of natural feeding in the field. Angelfish challenges they face, including consumption by fish departed from their usual ‘smorgasbord’ feeding (i.e. and starfish, smothering by sediments and breakage by continuously moving among sponge species) (Randall physical disturbance (e.g. Wulff 1997a). In such a con- & Hartman 1968; Wulff 1994) only for the two species text, directing resources to concerns other than rapid they consumed most readily. Parrotfish consumed a growth may make sense. sponge until it was gone or they were chased away, exactly The passage of a hurricane was reflected in lower as they feed on exposed cryptic reef sponges (Wulff survival of Pelican Cay sponges on the reef, but abiotic 1988, 1997b, 1997c). This is not the first report of reef conditions definitely did not inhibit sponges trans- fishes eating mangrove sponges. Gut contents of parrotfish planted between mangrove cays, as Twin Cays sponges feeding in mangroves contained spicules from one thrived inside cages (predator-free) in the Pelicans, and mangrove species (Dunlap & Pawlik 1998), and videos Pelican Cays sponges thrived on pvc pipes (competitor- of reef fishes feeding on chunks of mangrove sponges on free) at Twin Cays. exposed racks showed consumption of four species (Dunlap & Pawlik 1996), but details of normal feeding beha- viour were lost in feeding melees resulting from sudden appearances of large pieces of freshly cut sponges. If spongivores can inhabit Pelican Cays mangroves Restriction of species to refuges implies that a ‘refuge’ and prevent typical mangrove species from living there, is a less desirable place to live. Cryptic spaces in the reef why are these fishes absent from Twin Cays and other frame (Wulff 1988, 1997c) or under rubble (Dunlap & typical Caribbean mangrove stands? Three-dimensional Pawlik 1996) can constrain the size a sponge achieves, structure of the reefs in which Pelican Cays mangroves and referring to these as refuges may be reasonable for © 2005 British are embedded may offer fishes hiding places that are some species. Mangrove roots have also been considered Ecological Society, Journal of Animal not available in or near typical mangrove stands (Wulff refuges from predators (e.g. by Dunlap & Pawlik 1996; Ecology, 74, 2000 and additional personal observation). Barracudas Wulff 2000) for mangrove sponge species, although 313–321 are not absent from mangroves. additional experiments are required to determine if 319 mangrove sponges would grow and survive better in Negative associations of growth rate with defences Growth-defence other habitats if spongivores were eliminated. Faculta- can be interpreted in a variety of ways (see, e.g. Simms trade-offs and tive mutualism with mangroves may also inhibit habitat 1992) and are complicated by trade-offs among other sponge diversity switches of some mangrove species (Ellison, Farnsworth aspects of living (see, e.g. Mauricio 1998). Although & Twilley 1996). Data in this report do demonstrate, comparisons among species are confounded further by however, that sponge species that typically inhabit reefs differences in skeletal materials, modes of reproduction can grow and survive substantially better on mangrove and chemistry, and our virtually complete ignorance roots than on the reef (Fig. 2). However, the more rapid about how costly all these aspects of living actually are, growth of reef sponges on mangrove roots is insuffi- they can offer insight into influence of trade-offs on cient to prevent overgrowth by still more rapidly grow- community structure and function. ing 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. 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, A trade-off between growth rate and defence is sug- and many more await description. Sponges are dominant gested by the faster growth and more frequent partici- space-occupying organisms on reefs (e.g. Diaz & Rützler pation in overgrowth of the three mangrove species that 2001) and mangrove roots throughout the region were consumed most quickly by fishes; intermediate (e.g. Sutherland 1980; Ellison et al. 1996; Rützler et al. growth rates of less eagerly consumed mangrove spe- 2000; Wulff 2000). The key functional roles played by cies; and slow growth of the well-defended reef species sponges in these systems are not covered by other (except the unusual D. anchorata). Data on consump- organisms (Diaz & Rützler 2001; Wulff 2000). Under- tion of the typical reef species were not collected in this standing the relative importance of biotic and abiotic study because it takes years to accumulate sufficient factors in maintaining sponge diversity has become observations of natural feeding on well-defended sponges, crucial as conservation becomes more pressing. but a hint of an inverse relationship between growth Distinctiveness of sponge faunas in different habi- and defence is seen in data from a 12-year study of tats has been attributed to abiotic factors, with which unmanipulated angelfish feeding on a completely sponge distributions are often well correlated (see, censused sponge community. For the relatively quickly e.g.Wilkinson & Evans 1989; Diaz et al. 1990; Alcolado growing (Fig. 3) I. birotulata the ratio of number of 1994; Zea 1994). However, although abiotic differences bites taken to total volume of sponge tissue was 0·07 between coral reefs and mangroves are many and well (426 bites : 6001·3 cm3), while these ratios for the more correlated with differences in the sponge faunas, in this slowly growing A. fulva and A. compressa were only 0·02 first experimental test the causal relationship between (72 bites : 3626·3 cm3) and 0·01 (117 bites : 9767·3 cm3), abiotic factors and habitat distributions of sponge respectively (data from Wulff 1994 and unpublished). species is shown to be secondary. Trade-offs between growth and defence are well Within-habitat sponge diversity has also been attrib- studied for terrestrial plants (e.g. Messina et al. 2002 uted to abiotic factors. Negative influences have been and references therein), but directly relevant data are attributed to physical disturbance, sunlight and sedi- rare for clonal marine animals. The one direct study of mentation (see, e.g. Wilkinson & Evans 1989; Alvarez resource allocation in sponges (Becerro, Turon & Uriz et al. 1990; Zea 2001 and references therein). Positive 1995; Uriz et al. 1995) demonstrated shifts by the influences have been attributed to high substratum area, encrusting Mediterranean sponge Crambe crambe to low turbidity, and close proximity of propagule source greater investment in defensive and supportive struc- habitats (Rützler et al. 2000). It is probable that all of tures, at the expense of somatic growth and reproduction, these factors could influence sponge diversity, but the in environments where competition was important. contrasting systems in this study, with 2·5-fold dif- Another study (Hill 1998) has suggested that angel- ferences in species diversity (57 species at Twin Cays and fishes preferentially consume a sponge, Chondrilla 147 species in the Pelican Cays were reported by Rützler nucula, that may grow quickly; but angelfish preference et al. 2000), and in which competition or predation was assumed on the basis of gut content data (Randall strongly influence membership, suggest a look at how & Hartman 1968) which were not corrected for relative interactions might also influence within-habitat diversity. availability of sponge species. This sponge might In systems in which effectiveness at gaining space is © 2005 British overgrow corals if not consumed (Vicente 1990; Hill key to survival of sessile organisms, competitively dom- Ecological Society, Journal of Animal 1998), so confirmation of fast growth and of angelfish inant species may overwhelm all others, lowering diver- Ecology, 74, preference for this species would be especially sity. This expectation must be modified for systems 313–321 interesting. characterized by discontinuous habitat structure. 320 Sutherland (1980) pointed out that the discontinuous systems, the higher species diversity on coral reefs than J. L. Wulff substrata provided by mangrove roots can increase on mangroves has implied that the coral reef is the diversity by preventing space monopolization by com- superior habitat for tropical sponges. In fact, the higher petitive dominants across large continuous areas, a key diversity may reflect the multiple challenges that make insight that has subsequently aided understanding of living on a coral reef more of a struggle for sponges. many other systems. The outcome for the typical man- Mangroves, with higher nutrients, lower physical dis- grove root community is that diversity may be lowered turbance and no predators, offer typical reef sponges on a particular root as fast-growing species overwhelm better survival and growth, but trade-offs between others, but discontinuous substrata slow elimination defences and growth put this paradise out of reach as from the system, resulting in moderate overall species long as it is inhabited by typical mangrove species that diversity. have traded the ability to cope with challenges for the In contrast, in the Pelican Cays, where typical reef- ability to grow more rapidly. sponge species live on mangrove roots, spongivores may prevent community domination by faster-growing Acknowledgements sponge species. This mechanism for maintaining high diversity of sessile organisms was pointed out early on Fieldwork for this project was supported by the by studies of preferential consumption of competitive National Museum of Natural History’s Caribbean dominants by rabbits and starfish (Tansley & Adamson Coral Reef Ecosystems Program (CCRE Contribution 1925; Paine 1966). If an inverse relationship between no. 693). I am grateful for the vigorous discussion and growth rate and defences holds for more species than comradeship of fellow participants in the International the 12 most abundant ones chosen for these experi- Sponge Systematics Workshop convened at Carrie ments, predators are at least partly responsible for the Bow Cay in 1997. Thoughtful comments from J. Travis, exceptionally high sponge diversity of the typical N. Underwood, D. Ferrell, T. Swain and anonymous shallow coral reef sponge fauna. 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Sponges in Time and Space: Biology, Chemistry, Received 28 January 2004; accepted 13 August 2004 © 2005 British Ecological Society, Journal of Animal Ecology, 74, 313–321