Coral-Seaweed-Grazer-Nutrient Interactions on Temperate Reefs

Why corals dominate tropical reefs but are rare or absent on temperate reefs is one of the more intriguing global-scale questions in marine ecology. Restriction of corals from temperate reefs has been suggested to be due to low temperature, competition with seaweeds, and synergistic interactions of physical and biological factors. However, most studies addressing these hypotheses have been non-experimental and conducted on tropical corals and reefs near the extremes of their distribution rather than in temperate habitats using corals that are physiologically suited to temperate environments. Some corals occur only in temperate regions, but their ecology is largely unstudied. In an attempt to understand how temperate corals function at latitudes where corals are relatively rare and where reefs tend to be dominated by seaweeds, we examined responses of the temperate coral Oculina arbuscula to competition with seaweeds on reefs in North Carolina (USA). We asked how competitive interactions were affected by levels of grazing, nutrients, or interactions of these factors. Sampling of 12 reef habitats ranging from 1 m deep, inshore sites to 25 m deep, offshore sites demonstrated a strong negative relationship between percentage cover of seaweeds and density of Oculina colonies. Seaweeds dominated well-lit habitats (shallow inshore reefs or deep offshore reefs with clear waters), while coral was significantly more abundant in low-light habitats where seaweeds were rare (deep inshore habitats or nearshore reefs with turbid waters). This general among-site pattern also occurred within an individual site as one moved from shallow, well-lit waters to deeper, darker waters. Corals transplanted into seaweed-dominated areas grew well if seaweed canopies were removed but grew poorly, or not at all, if canopies were left intact. Seaweeds also significantly inhibited recruitment of 0. arbuscula. At a turbid inshore reef, re- cruitment was high at a depth of 6 m where seaweeds were rare, but very low at a depth of 1 m where seaweeds were abundant. Removal of seaweeds from shallow plots increased recruitment about 12-fold to levels that did not differ significantly from those at 6 m. In grazer-exclusion cages on offshore reefs, Oculina recruitment varied significantly between sites and years. Almost no recruitment was observed at a well-lit, plant-dominated site while recruitment was higher, to very high, at a turbid site with few seaweeds. At this turbid site, recruitment was facilitated by grazing but could not be related to grazer effects on seaweeds. Facilitation was apparently due to consumers removing barnacles, which dominated this low-light site if grazers were excluded. Cage exclusion of larger herbivores at two offshore sites (primarily fishes) and one inshore site (fishes and urchins) had no significant effect on coral growth. At the well-lit inshore site, herbivores had a large effect on the species composition of the seaweed community, but little effect on the total abundance of seaweeds. Large grazers caused palatable red seaweeds to be replaced by similar amounts of unpalatable brown seaweeds. Therefore, herbivory alone had little impact on total sea- weed abundance and the levels of seaweed competition affecting co-occurring 0. arbuscula. In contrast, when we conducted a factorial experiment manipulating both herbivory and nutrient levels, exclusion cages significantly reduced coral growth. In this experiment, nutrient addition had no effect on brown seaweeds but significantly increased the percentage cover of red seaweeds in ex- clusion cages. Nutrient addition also tended to suppress coral growth in herbivore-exclusion cages where red seaweeds were stimulated, but to increase coral growth in open cages where herbivores had removed the red seaweeds. Thus, nutrients and herbivory may have acted synergistically to affect seaweeds, and hence corals, on this temperate reef. Different groups of algae (red vs. brown) experienced differential degrees of nutrient limitation and exerted differential competitive effects on corals at this site. Our findings show that competition with seaweeds plays a large role in excluding Oculina from well-lit temperate reefs, and support the hypothesis that seaweed competition may interact with latitudinal changes in physical parameters to limit coral recruitment, growth, and accumulation at high latitudes, thus suppressing the potential for reef development.