Macroalgal blooms on southeast Florida coral reefs: Ⅱ. Cross-shelf discrimination of nitrogen sources indicates widespread assimilation of sewage nitrogen

摘要

Since 1990, coral reefs off southeast Florida have experienced an unprecedented succession of macroalgal blooms and invasions. To determine if anthropogenic land-based nitrogen (N) sources support these HABs, we collected macroalgal tissue for stable nitrogen isotope (δ~(15)N) analysis at three spatially distinct depths ranging from the shallow subtidal to the shelf break (～43 m) along seven transects from Jupiter to Deerfield Beach, Florida, USA. This sampling was initiated during a historically significant drought in the spring of 2001 when rainfall, stormwater runoff, and upwelling were at a minimum. The sampling was repeated in the summer wet season following significant stormwater runoff and during a strong upwelling event. Despite significant seasonal changes in N source availability, δ~(15)N values did not vary between samplings. Collectively, δ~(15)N values were significantly higher on inshore shallow reefs (+ 8.1 per thousand) compared to mid (+ 6.1 per thousand) and deep reefs (+ 6.7 per thousand). Values were also elevated in the southern portion of the study area (e.g., Boca Raton, + 8.5 per thousand) where nearly 1.5 billion l/day of secondarily treated wastewater is discharged into the ocean via coastal outfalls. Codium isthmocladum, a macroalga that assimilates its nutrients entirely from the water column, was the dominant bloom species in the southern study area, where tissue δ~(15)N values matched source values of nearby sewage outfalls. The northern study area was dominated by species of the genus Caulerpa, particularly the invasive Pacific native C. brachypus var. parvifolia, which are capable of accessing benthic nutrient sources (e.g., submarine groundwater discharge, SGD) by means of root-like rhizoids. The northern area does not have sewage outfalls but features a highly transmissive geologic zone where SGD may be enriched with septic tank leachate and effluent from municipal deep injection wells. Multiple lines of evidence supported the hypothesis that land-based sewage N was more important than upwelling as a N source to these HABs: (1) δ~(15)N values were highest on shallow reefs and decreased with increasing depth, indicating land-based sources of enrichment; (2) elevated δ~(15)N values occurred in these HABs during the dry season, prior to the onset of the summer upwelling; (3) elevated NH_4~+ concentrations occur on these reefs during both upwelling and non-upwelling periods and are kinetically preferred by macroalgae compared to upwelled NO_3~-. These findings provide a case study of a coupling between increasing anthropogenic activities and the development of macroalgal HABs, including invasive species that threaten economically important reef resources in southeast Florida.