Consumptive and non-consumptive effects of invasive lionfish on native herbivores: potential consequences for ecological resilience of coral reefs
On Caribbean coral reefs, herbivorous fishes (especially parrotfishes) foster coral dominance by reducing the deleterious effects of benthic algae on corals. Reduced stocks of herbivorous fishes from overfishing can result in algae displacing corals and impairing reef resilience. Similarly, the voracious invasive red lionfish (Pterois volitans) could reduce herbivorous fish populations via direct predation (i.e., “consumptive effects” or CEs), as well as by inhibiting fish grazing behavior (i.e., “non-consumptive effects” or NCEs). We tested for CEs and NCEs of invasive lionfish on native herbivorous fish populations and grazing behavior, respectively. In June 2009, we manipulated lionfish density (low and high) on 10 paired large reefs in the Bahamas. We surveyed fish populations and maintained lionfish treatments every 3-5 months thereafter. In July 2011, we quantified fish grazing behavior (visitation and bite rates) on algal-covered substrata placed in microhabitats differing in lionfish presence at the time of observation at the reef (low and high lionfish density) and within-reef scales (lionfish presence-absence in microhabitat): (1) low-lionfish-density reef with lionfish absent from microhabitat; (2) high-lionfish-density reef with lionfish absent from microhabitat; and (3) high-lionfish-density reef with lionfish present in microhabitat. We also quantified algal loss per substrate from observed grazing from before-and-after photographs.
Linear mixed effects models revealed that, over the two-year experiment, lionfish significantly reduced the density of small herbivorous fishes by the end of the 2009 recruitment season (lionfish × time interaction: LRT P=0.002); small parrotfishes responded similarly (lionfish × time interaction: LRT P = 0.017). Lionfish also significantly reduced the grazing activity of both small and large herbivorous fishes (all variables: LRT P < 0.001). Parrotfishes were the only fish family whose grazing behavior was affected by lionfish (all variables: LRT P < 0.001). When lionfish were present on reefs, lionfish indirectly reduced algal loss of substrata by 66-80%. Thus, there was clear evidence of an invasive marine predator having both CEs and NCEs on native herbivores. These findings suggest that invasive lionfish diminish the functional role of herbivorous fish grazing on native reefs, especially parrotfishes, thereby reducing ecological resilience and rendering corals more susceptible to overgrowth by seaweeds.