Top-down modification of bottom-up processes: selective grazing reduces macroalgal nitrogen uptake

Although nutrient availability and oceanographic context can influence top-down processes in intertidal communities, the reciprocal effects of consumers on bottom-up processes, such as nitrogen uptake by macroalgae, are less well-documented. We used a combination of field observations, mesocosm experiments, and laboratory nitrate-uptake measurements to evaluate the interaction between the kelp crab Pugettia producta and its preferred food source, the kelp Egregia menziesii, in northern California, USA. We found that R producta fed selectively on E. menziesii, removing tissues with a high surface area to volume ratio (SA:V), which resulted in a 66% decrease in overall SA:V. Because these high SA:V tissues are disproportionately more responsible for nitrate uptake, selective herbivory by P. producta decreased E. menziesii's biomass-specific uptake of nitrogen, the primary limiting nutrient in this ecosystem, by 65% per gram of remaining algal tissue. In field surveys, where P. producta abundances were high, E. menziesii thalli more frequently exhibited signs of intense grazing and thus had lower SA:V ratios, suggesting that grazing is sufficiently intense in the field to generate differences in algal morphology and nitrate uptake. P. producta therefore influences E. menziesii biomass and productivity from the top down, by removing substantial amounts of biomass, and from the bottom up, by reducing the kelp's subsequent ability to acquire nutrients. Because of selective grazing on specialized tissues, the effects of mesoherbivores, like P. producta, on the structure and dynamics of marine communities may often be greater than predicted simply by the biomass they consume.