Macroalgae respond to consumer-mediated nutrient cycling in a temperate ecosystem

Primary production in coastal upwelling regions has often been presumed to be supported primarily by allochthonous nutrients, but inconsistent nutrient delivery and the metabolic cost of nitrate assimilation can leave producers nitrogen limited during the growing season. As a potential supplement for insufficient allochthonous supply, nutrient provisioning through the metabolic wastes of animals, termed consumer-mediated nutrient cycling (CNC), provides easily assimilated nitrogen in the form of ammonium. Although it has been suggested that CNC sustains macroalgal growth on the west coast of North America, experimental fertilization experiments, especially on kelps, are lacking. Here, we measured the growth rates of winged kelp (Alaria marginata) and sea lettuce (Ulva sp.) under ammonium levels that varied experimentally in the laboratory as well as naturally across sites in the wild. We observed evidence that in the field, a regionally high-nitrate environment, elevated ammonium was associated with 1.4× higher growth and 1.2× higher percent nitrogen content in A. marginata. Using in situ mesocosms, we observed that Ulva grew 3.8× faster and had 1.4× higher internal nitrogen concentration when exposed to nitrogen-rich excretion from red rock crabs (Cancer productus). Our study suggests kelps growing in low ammonium but higher nitrate conditions may be nitrogen limited, suggesting that nitrates from allochthonous sources may not meet the nutrient requirements of macroalgae in this moderate upwelling ecosystem. Therefore, nutrient regeneration by animals may be an important source of nitrogen across varying levels of allochthonous nitrate supply.