A review of bottom-up vs. top-down control of sponges on Caribbean fore-reefs: what’s old, what’s new, and future directions

Abstract

Interest in the ecology of sponges on coral reefs has grown in recent years with mounting evidence that sponges are becoming dominant members of reef communities, particularly in the Caribbean. New estimates of water column processing by sponge pumping activities combined with discoveries related to carbon and nutrient cycling have led to novel hypotheses about the role of sponges in reef ecosystem function. Among these developments, a debate has emerged about the relative effects of bottom-up (food availability) and top-down (predation) control on the community of sponges on Caribbean fore-reefs. In this review, we evaluate the impact of the latest findings on the debate, as well as provide new insights based on older citations. Recent studies that employed different research methods have demonstrated that dissolved organic carbon (DOC) and detritus are the principal sources of food for a growing list of sponge species, challenging the idea that the relative availability of living picoplankton is the sole proxy for sponge growth or abundance. New reports have confirmed earlier findings that reef macroalgae release labile DOC available for sponge nutrition. Evidence for top-down control of sponge community structure by fish predation is further supported by gut content studies and historical population estimates of hawksbill turtles, which likely had a much greater impact on relative sponge abundances on Caribbean reefs of the past. Implicit to investigations designed to address the bottom-up vs. top-down debate are appropriate studies of Caribbean fore-reef environments, where benthic communities are relatively homogeneous and terrestrial influences and abiotic effects are minimized. One recent study designed to test both aspects of the debate did so using experiments conducted entirely in shallow lagoonal habitats dominated by mangroves and seagrass beds. The top-down results from this study are reinterpreted as supporting past research demonstrating predator preferences for sponge species that are abundant in these lagoonal habitats, but grazed away in fore-reef habitats. We conclude that sponge communities on Caribbean fore-reefs of the past and present are largely structured by predation, and offer new directions for research, such as determining the environmental conditions under which sponges may be food-limited (e.g., deep sea, lagoonal habitats) and monitoring changes in sponge community structure as populations of hawksbill turtles rebound.

Spongivory by Fishes on Southwestern Atlantic Coral Reefs: No Evidence of Top-Down Control on Sponge Assemblages

“…In Caribbean reefs sponge assemblages have been found to be primarily controlled by predatory reef fishes (Pawlik et al, 2013) and by hawksbill turtles (Pawlik et al, 2018). The biodiversity and abundance of spongivorous fishes and sponges in Caribbean reefs are considerably higher than in Southwestern Atlantic reefs (Roberts et al, 2002;van Soest et al, 2012).…”

“…The relative high sponge cover found in TSB may be associated with availability of particulate food as picoplankton (Lesser, 2006;Lesser and Slattery, 2013) and dissolved organic carbon (DOC), both important resources used by sponges (de Goeij et al, 2013;Poppell et al, 2014;Pawlik et al, 2015Pawlik et al, , 2018. Local aspects of TSB such as natural and anthropic nutrient inputs and picoplankton availability may favor or control sponge assemblages.…”

“…Top-down or bottom-up control of sponge assemblages in coral reefs is an important contemporary discussion (e.g., Pawlik et al, 2018). An evidence for top-down control in TSB reefs would be if sponge cover in sites with higher angelfish density were smaller than in sites with low angelfish (spongivorous) densities.…”

“…Evidences in high diversity coral reefs, such as Caribbean reefs, showed that top-down regulation by fish play a decisive role on growth of different sponge species, consequently affecting benthic assemblages (Dunlap and Pawlik, 1996;Pawlik, 1997Pawlik, , 1998Pawlik et al, 2013Pawlik et al, , 2018. Brazilian coral reefs have peculiar features as relatively low coral diversity, high sedimentation rates and elevated turbidity due to abundant river flow into shore.…”

“…Different approaches have been used to investigate the potential effect of predation by reef fishes, for instance by using stomach content analysis (Randall and Hartman, 1968;Andréa et al, 2007;Reis et al, 2013) and fish feeding activity observations (Longo and Floeter, 2012;Pratchett et al, 2014). Although there is information about fish predation pressure on sponge assemblages (Pawlik et al, 2018), little is known about the spongivorous fish foraging behavior. Foraging activity is an essential aspect of habitat use by fishes and a predominant daily activity.…”