Bottom-up and top-down controls on coral reef sponges: disentangling within-habitat and between-habitat processes

Polarized debates about top-down vs. bottom-up control have given way to more nuanced understanding of control by both resources and consumers in many systems, but coral reef sponges have recently been asserted to differ from other groups in being controlled exclusively top-down. This assertion has been countered by reports of exclusively bottom-up control, with both conclusions based on studies of the same species. Accelerating deterioration of coral reefs motivates knowing the contexts in which either consumers or nutrients or both control key ecosystem role players like sponges. Accordingly, genotype- and size-controlled individuals of 12 common Caribbean reef sponge species were transplanted, in the field, into five circumstances differing in predators, competitors, and the picoplankton consumed by sponges. Growth and survival of the experimental transplants for periods of 1-9 yr revealed context-dependent control of sponges. Primary control of growth was bottom-up, with more picoplankton resulting in consistent and sustained higher growth rates for all 12 of these ecologically and phylogenetically diverse species. Top-down control was not detected within-habitat, on the coral reef. However, between-habitat control was by predation and competition, with reef sponges excluded from adjacent seagrass meadows by spongivorous starfish, and excluded from mangrove prop roots by faster-growing mangrove sponges. These results highlight the strong importance of experimental design details that consider behavior idiosyncrasies, sufficiently long time scales, and appropriate division of species into categories. Diametrically opposite results from studies of the same species also illustrate the inherently greater difficulty of detecting bottom-up processes and the importance of distinguishing within-habitat vs. between-habitat patterns and processes.