Sediment-mediated suppression of herbivory on coral reefs: Decreasing resilience to rising sea levels and climate change?

We describe a mechanistic basis for maintaining an alternative degraded stable state on coral reefs: sedimentladen algal turfs. Using remote underwater video cameras we quantified rates of herbivory by coral reef fishes on epilithic algal turfs with natural and experimentally reduced sediment loads. Removal of sediment increased overall fish feeding rates 3.8-fold, and resulted in a decrease in mean algal turf length of 64% within 4 h. After 4 h, sediment accumulated in the treatment plots, but only returned to 41% of the original depth. A total of 20 species actively fed on the sediment removal plots, compared with 12 species in control plots. Of the five numerically abundant herbivorous fish species, all increased feeding by at least 225% in the absence of sediment. Only juvenile Scarus spp. fed to any extent (28% of bites) on control plots. We suggest that naturally occurring sediment loads in epilithic algal turfs can suppress herbivory and that sediment-laden algal turfs may be an alternative stable state on coral reefs. This may provide a mechanistic basis for the geological evidence of a sediment-induced turn-off of coral reef growth. With projected global sea-level rises due to climate change, reef-based sediment loads may be a critical factor in differentiating the relative resilience of coral reefs and identifying reef ecosystems that are at highest risk to rising sea levels. Throughout the world’s tropical oceans there is increasing evidence of detrimental changes on coral reefs. In many areas coral reefs are exhibiting a progressive deterioration as systems become increasingly affected by human activities such as overfishing, habitat loss, or increased terrigenous input (Hughes et al. 2003; Pandolfi et al. 2003). Some of these areas exhibit more catastrophic changes marked by phase shifts, where the system flips rapidly from one ecosystem state to another (McClanahan et al. 2001; Bellwood et al. 2004). In many cases these changes have been associated with, or are exacerbated by, global climate change (Hughes et al. 2003). For coral reefs, ecosystem changes, whether gradual or rapid, are often associated with a shift from a coraldominated to an algal-dominated state. One of the most widely recognized shifts is the coral–macroalgal phase shift, which has been reported on reefs from the tropical Atlantic, Indian, and Pacific oceans (McClanahan et al. 2001; McCook et al. 2001; Mumby et al. 2006). However, this is only one of a range of possible ecosystem transitions on coral reefs (Bellwood et al. 2004). Which of these states or transitions occurs is dependent on both the biological and physical environment. Although coral reef deterioration is often marked by a shift to a macroalgal-dominated state, this can only occur within certain constraints. Tropical macroalgae have specific limitations shaped by their depth, light, and sediment tolerance and their susceptibility to wave-induced water motion (Hay 1981; Steneck and Dethier 1994). Moreover, algal distribution is strongly shaped by patterns of herbivory, especially fish herbivory (McCook et al. 2001; Burkepile and Hay 2006; Littler et al. 2006). Similar constraints apply to crustose coralline and epilithic ‘‘turf’’ algae (Steneck and Dethier 1994; Airoldi 1998, 2003). On both Indo-Pacific and Caribbean coral reefs, large areas of substratum are covered by an algal turf or epilithic algal matrix (EAM; Wilson et al. 2003); on flat open areas this is often manifested as a sediment-rich epilithic algal turf or ‘‘hard pan’’ (Steneck et al. 1997; Purcell and Bellwood 2001). This substratum configuration often appears to be a relatively stable state (Kench and Brander 2006), with little evidence of it being a transitory state shifting to coral, crustose coralline, or macroalgal domination, at least in the short term. Although this type of benthic cover may be expected in areas with low herbivore densities, why such habitats persist in herbivore-rich areas, such as mid-shelf reefs on the Great Barrier Reef (GBR), is unclear. How can 1–2-cm-thick epilithic algal mats persist on coral reefs in areas with a high density and diverse array of mobile fish herbivores? It has been suggested that some sediment types on coral reefs can act as a deterrent to herbivory and that herbivory 1 Corresponding author ([email protected]). Acknowledgments We thank the staff of Lizard Island Research Station, A. Gonzalez-Cabello, J. Johansen, and R. Kushner for field assistance; A. Hoey, J. H. Choat, S. Wismer, and P. Kench for helpful discussions; and two anonymous reviewers for valuable comments on the manuscript. This work was supported by the Australian Research Council. Limnol. Oceanogr., 53(6), 2008, 2695–2701 E 2008, by the American Society of Limnology and Oceanography, Inc.