Frequent disturbance to a foundation species disrupts consumer-mediated nutrient cycling in giant kelp forests

Abstract

Structure-forming foundation species facilitate consumers by providing habitat and refugia. In return, consumers can benefit foundation species by reducing top-down pressures and increasing the supply of nutrients. Consumer-mediated nutrient dynamics (CND) fuel the growth of autotrophic foundation species and generate more habitat for consumers, forming reciprocal feedbacks. Such feedbacks are threatened when foundation species are lost to disturbances, yet testing these interactions requires long-term studies, which are rare. Here, we experimentally evaluated how disturbance to giant kelp, a marine foundation species, affects (1) CND of the forest animal community and (2) nutrient feedbacks that help sustain forest primary production during extended periods of low nitrate. Our experiment involved removing giant kelp annually during the winter for 10 years at four sites to mimic frequent wave disturbance. We paired temporal changes in the forest community in kelp removal and control plots with estimates of taxon-specific ammonium excretion rates (reef fishes and macroinvertebrates) and nitrogen (N) demand (giant kelp and understory macroalgae) to determine the effects of disturbance on CND as measured by ammonium excretion, N demand by kelp forest macroalgae, and the percentage of nitrogen demand met by ammonium excretion. We found that disturbance to giant kelp decreased ammonium excretion by 66% over the study, mostly due to declines in fishes. Apart from a few fish species that dominated CND, most reef-associated consumers were unaffected by disturbance. Disturbance to giant kelp reduced its N demand by 56% but increased that of the understory by 147% due to its increased abundance in the absence of a kelp canopy. Overall, disturbance had little effect on the fraction of N demand of macroalgae met by consumer excretion due to the offsetting responses of giant kelp, understory macroalgae, and consumers to disturbance. Across both disturbance regimes, on average, consumers supported 11%–12% of the N required by all kelp forest macroalgae and 48% of N demand by the understory macroalgae (which are confined to the benthos where most reef-associated consumers reside). Our findings suggest that CND constitutes a considerable contribution of N required in kelp forests, yet nutrient inputs decrease following reductions in essential habitat perpetuated by frequent disturbances.