Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA: a 3-decade study

Abstract

Increased loadings of nitrogen (N) from fertilizers, top soil, sewage, and atmospheric deposition are important drivers of eutrophication in coastal waters globally. Monitoring seawater and macroalgae can reveal long-term changes in N and phosphorus (P) availability and N:P stoichiometry that are critical to understanding the global crisis of coral reef decline. Analysis of a unique 3-decade data set for Looe Key reef, located offshore the lower Florida Keys, showed increased dissolved inorganic nitrogen (DIN), chlorophyll a, DIN:soluble reactive phosphorus (SRP) ratios, as well as higher tissue C:P and N:P ratios in macroalgae during the early 1990s. These data, combined with remote sensing and nutrient monitoring between the Everglades and Looe Key, indicated that the significant DIN enrichment between 1991 and 1995 at Looe Key coincided with increased Everglades runoff, which drains agricultural and urban areas extending north to Orlando, Florida. This resulted in increased P limitation of reef primary producers that can cause metabolic stress in stony corals. Outbreaks of stony coral disease, bleaching, and mortality between 1995 and 2000 followed DIN enrichment, algal blooms, and increased DIN:SRP ratios, suggesting that eutrophication interacted with other factors causing coral reef decline at Looe Key. Although water temperatures at Looe Key exceeded the 30.5 °C bleaching threshold repeatedly over the 3-decade study, the three mass bleaching events occurred only when DIN:SRP ratios increased following heavy rainfall and increased Everglades runoff. These results suggest that Everglades discharges, in conjunction with local nutrient sources, contributed to DIN enrichment, eutrophication, and increased N:P ratios at Looe Key, exacerbating P limitation, coral stress and decline. Improved management of water quality at the local and regional levels could moderate N inputs and maintain more balanced N:P stoichiometry, thereby reducing the risk of coral bleaching, disease, and mortality under the current level of temperature stress.

Full text

Vol.:(0123456789)
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Marine Biology (2019) 166:108
https://doi.org/10.1007/s00227-019-3538-9
HIGHLIGHT ARTICLE
Nitrogen enrichment, altered stoichiometry, andcoral reef decline
atLooe Key, Florida Keys, USA: a3‑decade study
BrianE.Lapointe1 · RachelA.Brewton1 · LauraW.Herren1 · JamesW.Porter2 · ChuanminHu3
Received: 8 February 2019 / Accepted: 3 June 2019 / Published online: 15 July 2019
© Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Increased loadings of nitrogen (N) from fertilizers, top soil, sewage, and atmospheric deposition are important drivers
of eutrophication in coastal waters globally. Monitoring seawater and macroalgae can reveal long-term changes in N and
phosphorus (P) availability and N:P stoichiometry that are critical to understanding the global crisis of coral reef decline.
Analysis of a unique 3-decade data set for Looe Key reef, located offshore the lower Florida Keys, showed increased dis-
solved inorganic nitrogen (DIN), chlorophyll a, DIN:soluble reactive phosphorus (SRP) ratios, as well as higher tissue C:P
and N:P ratios in macroalgae during the early 1990s. These data, combined with remote sensing and nutrient monitoring
between the Everglades and Looe Key, indicated that the significant DIN enrichment between 1991 and 1995 at Looe Key
coincided with increased Everglades runoff, which drains agricultural and urban areas extending north to Orlando, Florida.
This resulted in increased P limitation of reef primary producers that can cause metabolic stress in stony corals. Outbreaks of
stony coral disease, bleaching, and mortality between 1995 and 2000 followed DIN enrichment, algal blooms, and increased
DIN:SRP ratios, suggesting that eutrophication interacted with other factors causing coral reef decline at Looe Key. Although
water temperatures at Looe Key exceeded the 30.5°C bleaching threshold repeatedly over the 3-decade study, the three mass
bleaching events occurred only when DIN:SRP ratios increased following heavy rainfall and increased Everglades runoff.
Theseresults suggest that Everglades discharges, in conjunction with local nutrient sources, contributed to DIN enrichment,
eutrophication, and increased N:P ratios at Looe Key, exacerbating P limitation, coral stress and decline. Improved manage-
ment of water quality at the local and regional levels could moderate N inputs and maintain more balanced N:P stoichiometry,
thereby reducing the risk of coral bleaching, disease, and mortality under the current level of temperature stress.
Introduction
Coral reefs have evolved over hundreds of millions of years
and are now considered one of the most threatened eco-
systems on our planet (Birkeland 1997, 2004; MEA 2005;
Hughes etal. 2017). These biologically diverse ecosystems
have been in decline globally since the 1970s due to a grow-
ing number of recognized stressors (Hughes etal. 2003;
Wilkinson 2004). In the Caribbean basin, an estimated 40%
of coral has been lost over the last 40years (Gardner etal.
2003) and similar losses have been observed along the Great
Barrier Reef, Australia (Bellwood etal. 2004; De’ath etal.
2012). Early studies focused largely on the effects of land-
based nutrient pollution and eutrophication (Banner 1974;
Tomascik and Sander 1987; Smith etal. 1981; Bell 1992;
Lapointe and Clark 1992), which was considered a primary
threat to coral reef health in the late 1980s (NOAA 1988;
Ginsburg 1994). Since then, overfishing (Hughes 1994;
Jackson etal. 2001), sedimentation (Rogers 1990; Fab-
ricius 2005), increases in sea surface temperature (Goreau
and Hayes 1994; Glynn 1996; Baker etal. 2008; Selig etal.
2012; Hughes etal. 2017), and ocean acidification (Kley-
pas etal. 2006; Hoegh-Guldberg etal. 2007; Muehllehner
etal. 2016) have emerged as additional threats to coral reefs.
While the potential for negative impacts (both direct and
Responsible Editor: S. Shumway.
Reviewed by undisclosed experts.
* Brian E. Lapointe
blapoin1@fau.edu
1 Harbor Branch Oceanographic Institute, Florida Atlantic
University, 5600 US-1, FortPierce, FL34946, USA
2 Odum School ofEcology, University ofGeorgia, Athens,
GA30602, USA
3 College ofMarine Science, University ofSouth Florida,
St.Petersburg, FL33701, USA
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