Chemical defenses and resource trade-offs structure sponge communities on Caribbean coral reefs

Abstract

Ecological studies have rarely been performed at the community level across a large biogeographic region. Sponges are now the primary habitat-forming organisms on Caribbean coral reefs. Recent species-level investigations have demonstrated that predatory fishes (angelfishes and some parrotfishes) differentially graze sponges that lack chemical defenses, while co-occurring, palatable species heal, grow, reproduce, or recruit at faster rates than defended species. Our prediction, based on resource allocation theory, was that predator removal would result in a greater proportion of palatable species in the sponge community on overfished reefs. We tested this prediction by performing surveys of sponge and fish community composition on reefs having different levels of fishing intensity across the Caribbean. A total of 109 sponge species was recorded from 69 sites, with the 10 most common species comprising 51.0% of sponge cover (3.6-7.7% per species). Nonmetric multidimensional scaling indicated that the species composition of sponge communities depended more on the abundance of sponge-eating fishes than geographic location. Across all sites, multiple-regression analyses revealed that spongivore abundance explained 32.8% of the variation in the proportion of palatable sponges, but when data were limited to geographically adjacent locations with strongly contrasting levels of fishing pressure (Cayman Islands and Jamaica; Curaçao, Bonaire, and Martinique), the adjusted R(2) values were much higher (76.5% and 94.6%, respectively). Overfishing of Caribbean coral reefs, particularly by fish trapping, removes sponge predators and is likely to result in greater competition for space between faster-growing palatable sponges and endangered reef-building corals.

Keywords: chemical ecology; community structure; indirect effects; marine protected areas; trophic dynamics.

Fig. 1.

Map of sites across the Caribbean where surveys were performed of sponge and fish community composition. Shading of site markers indicates abundance of sponge-eating fishes based on survey data using spongivore index (SI) (Dataset S3). Black, overfished (SI < 10); gray, intermediate (11 ≤ SI ≤ 20); white, protected (SI ≥ 21). Overlapping markers have been displaced for clarity.

Fig. 2.

Pooled percentages of chemically defended, consistently undefended, and variably defended sponges (the last two stacked as palatable sponges) at each survey location with the mean abundance of spongivorous fish (corrected for fish size) within 2,000 m³ of seawater directly above the reef. Sites that were designated as no-take fishing preserves were separated from the other survey sites for Puerto Rico and St. Lucia. Error bars denote SEs.

Fig. 3.

Correspondence analysis of survey sites for occurrences of chemically defended, consistently undefended, and variably defended sponges, and corrected total abundance of sponge predators within 2,000 m³ of seawater directly above the reef. Prefixes of site names denote the following locations: B, Bahamas; C, Cayman Islands; D, Dominican Republic; E, St. Eustatius; F, Key Largo, FL; J, Jamaica; M, Martinique; O, Bonaire; P, Bocas del Toro, Panama; R, Puerto Rico; S, St. Lucia; U, Curaçao; X, Mexico.

Fig. 4.

Fistularin 3, a brominated tyrosine-derived alkaloid and defensive metabolite that has the highest concentration in the tissues of the most abundant sponge, Aplysina cauliformis, based on the surveys conducted in this study. This compound and a complex mixture of related metabolites found in species of the genera Aplysina, Aiolochroia, and Verongula (24) constitute the most common chemical defense of Caribbean sponges.