ArticlePublisher preview available

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

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

Abstract and Figures

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.
This content is subject to copyright. Terms and conditions apply.
Vol.:(0123456789)
1 3
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
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... changes in the coral microbiome), making them more susceptible to infection, or the conditions increase the virulence or abundance of pathogens (Muller and Van Woesik, 2012). Exceeding such environmental thresholds will likely become increasingly common in rapidly warming oceans (Muller and Van Woesik, 2012) and more eutrophic waters (Lapointe et al., 2019), leading to more frequent coral disease outbreaks. Akumal Reef, impacted by coastal development and several bleaching events in the last decades, clearly shows the effects of coral disease prevalence in all years monitored from 1999 to 2021. ...
... Thus, the ability to understand the environmental threshold that drives coral disease activity in space and time, and therefore accurately predict the prevalence of coral diseases, is essential for practicing bestmanagement strategies that may reduce the influence of disease on coral reefs (Muller and Van Woesik, 2012). For example, the altered nitrogen and phosphorus stoichiometry can cause phosphorus starvation in corals and exacerbate the effects of high temperature on coral bleaching and coral disease (Lapointe et al., 2019). Improved management of water quality at the local and regional levels could moderate nitrogen inputs and maintain more balanced nitrogen and phosphorus stoichiometry (Lapointe et al., 2019), thereby reducing the risk of coral mortality and reef degradation, enhancing coral reef resilience to face multiple global and local stressors. ...
... For example, the altered nitrogen and phosphorus stoichiometry can cause phosphorus starvation in corals and exacerbate the effects of high temperature on coral bleaching and coral disease (Lapointe et al., 2019). Improved management of water quality at the local and regional levels could moderate nitrogen inputs and maintain more balanced nitrogen and phosphorus stoichiometry (Lapointe et al., 2019), thereby reducing the risk of coral mortality and reef degradation, enhancing coral reef resilience to face multiple global and local stressors. ...
Article
Coral diseases acting synergistically with other environmental stressors are a growing problem for Caribbean reefs. Hard coral cover, coral traits, and coral diseases were examined from 1999 to 2021 for Akumal reef, located in the Northern Mexican Caribbean. The 45 recorded coral species were classified into life-history strategies: competitive, stress-tolerant, and weedy, associated with different framework-building capacities. Results indicate that cumulative impacts of coral diseases outbreaks in the last two decades, in synergy with the effects of coastal development and thermal stressors, have decreased significantly cover and abundance of major reef-building corals, shifting the dominance of the coral assemblage to species belonging to non-framework weedy life history strategy, corresponding to a low Reef Functional Index. Due to the relevant role of coral diseases in shaping coral assemblages, addressing current, and preventing future coral disease outbreaks through integrated management strategies, will be paramount to preserving physical functionality in Caribbean reefs.
... changes in the coral microbiome), making them more susceptible to infection, or the conditions increase the virulence or abundance of pathogens (Muller and Van Woesik, 2012). Exceeding such environmental thresholds will likely become increasingly common in rapidly warming oceans (Muller and Van Woesik, 2012) and more eutrophic waters (Lapointe et al., 2019), leading to more frequent coral disease outbreaks. Akumal Reef, impacted by coastal development and several bleaching events in the last decades, clearly shows the effects of coral disease prevalence in all years monitored from 1999 to 2021. ...
... Thus, the ability to understand the environmental threshold that drives coral disease activity in space and time, and therefore accurately predict the prevalence of coral diseases, is essential for practicing bestmanagement strategies that may reduce the influence of disease on coral reefs (Muller and Van Woesik, 2012). For example, the altered nitrogen and phosphorus stoichiometry can cause phosphorus starvation in corals and exacerbate the effects of high temperature on coral bleaching and coral disease (Lapointe et al., 2019). Improved management of water quality at the local and regional levels could moderate nitrogen inputs and maintain more balanced nitrogen and phosphorus stoichiometry (Lapointe et al., 2019), thereby reducing the risk of coral mortality and reef degradation, enhancing coral reef resilience to face multiple global and local stressors. ...
... For example, the altered nitrogen and phosphorus stoichiometry can cause phosphorus starvation in corals and exacerbate the effects of high temperature on coral bleaching and coral disease (Lapointe et al., 2019). Improved management of water quality at the local and regional levels could moderate nitrogen inputs and maintain more balanced nitrogen and phosphorus stoichiometry (Lapointe et al., 2019), thereby reducing the risk of coral mortality and reef degradation, enhancing coral reef resilience to face multiple global and local stressors. ...
... Over the past four decades, numerous studies have identified the trend of continuous coral reef degradation due to natural and anthropogenic pressures. These pressures include enhanced local pollution of coastal areas (Burke et al. 2011;Häder et al. 2020;Randazzo-Eisemann et al. 2021), overfishing (Moussa et al. 2019;Nichols et al. 2019), destructive fishing practices (Yasir Haya and Fujii 2020;Hampton-Smith et al. 2021), sea surface temperature (Hughes et al. 2018;Ngoc 2019), climate change and subsequent ocean warming (Pendleton et al. 2016;Hughes et al. 2017Zhang et al. 2021, ocean acidification (Allemand and Osborn 2019;Zunino et al. 2021), coral diseases (Lapointe et al. 2019;Hazraty-Kari et al. 2021), nutrient enrichment (Lapointe et al. 2019;Adam et al. 2021), and other anthropogenic threats (Burke et al. 2011;Mellin et al. 2016;Hoegh-Guldberg et al. 2019;Hein et al. 2021). Degradation of coral reefs leads to a loss of their ecological and economic value, particularly the goods and services to coastal and other communities (Cesar and Chong 2004;Mehvar et al. 2018;Yasir Haya and Fujii 2019;Santavy et al. 2021). ...
... Over the past four decades, numerous studies have identified the trend of continuous coral reef degradation due to natural and anthropogenic pressures. These pressures include enhanced local pollution of coastal areas (Burke et al. 2011;Häder et al. 2020;Randazzo-Eisemann et al. 2021), overfishing (Moussa et al. 2019;Nichols et al. 2019), destructive fishing practices (Yasir Haya and Fujii 2020;Hampton-Smith et al. 2021), sea surface temperature (Hughes et al. 2018;Ngoc 2019), climate change and subsequent ocean warming (Pendleton et al. 2016;Hughes et al. 2017Zhang et al. 2021, ocean acidification (Allemand and Osborn 2019;Zunino et al. 2021), coral diseases (Lapointe et al. 2019;Hazraty-Kari et al. 2021), nutrient enrichment (Lapointe et al. 2019;Adam et al. 2021), and other anthropogenic threats (Burke et al. 2011;Mellin et al. 2016;Hoegh-Guldberg et al. 2019;Hein et al. 2021). Degradation of coral reefs leads to a loss of their ecological and economic value, particularly the goods and services to coastal and other communities (Cesar and Chong 2004;Mehvar et al. 2018;Yasir Haya and Fujii 2019;Santavy et al. 2021). ...
Article
Full-text available
In Indonesia, the coral reef ecosystem in the Tiworo Strait Conservation Area (TSCA) faces various threats of natural and anthropogenic stressors that can damage the coral reef ecosystem's role and services. We analyzed changes in coral reef habitat at TSCA over the 25 years from 1994 to 2019 using multi-temporal and multi-sensor satellite imagery data combined with in-situ measurement data and social surveys. Our results show a decrease in live coral cover from 78.30 ha in 1994 to 8.01 ha in 2019, with a 2.81 ha/year degradation rate. Our analysis of 37 threat attributes shows that the TSCA coral reef ecosystem faces a “high threat” to very high threat levels. Threat scores for coral reefs assessed as facing severe conditions according to threat indices included contributions from the ecological dimension (16.87 = very high threat), economic dimension (31.00 = high threat), social dimension (34.83 = high threat), technological dimension (41.10 = high threat), and law and institutional dimension (26.83 = high threat). Coral reefs will undoubtedly go extinct if local threats continue without preventative measures. Therefore, the sustainability of coral reefs in the TSCA—one of the most important marine conservation sites in the Coral Triangle Marine Eco-region should be the primary priority for all stakeholders. Appropriate policies and supervision in the field must be carried out rigorously and measurably, implementing the analyzed set of strategies.
... This uncertainty is of concern as the nutrient environments in coral reefs are likely to undergo continued change due to direct anthropogenic impact and climate change. Such changes may occur in the form of nutrient enrichment (Elizalde-Rendón et al. 2010;Browne et al. 2015), skewed N:P stoichiometries (D'Angelo and Wiedenmann, 2014;Lapointe et al. 2019) or nutrient depletion (Sun et al. 2008;Rosset et al. 2017). Accordingly, varied effects on coral skeletons can be expected, which may influence the formation of the 3-dimensional reef framework that is critically important for reef biodiversity and productivity (Purkis et al. 2008;Graham and Nash 2013), and coastal protection (Sheppard et al. 2005). ...
... Critically, a recent study shows that N:P ratios of macroalgae in the Belize Barrier Reef increased from ~30:1 in the 1980s to 70:1, indicating that a skewed N:P stoichiometry coincided with dramatic reductions in live coral cover (Lapointe et al. 2021). Also, Lapointe et al. (2019) linked coral reef decline at Looe Key, Florida to an increase in N:P from 9.5 to 26.5. Our findings, alongside those of previous studies (Wiedenmann et al. 2013;Rosset et al. 2017), have identified a physiological mechanism to explain such detrimental effects on reef building corals. ...
Article
Full-text available
Reported divergent responses of coral growth and skeletal microstructure to the nutrient environment complicate knowledge-based management of water quality in coral reefs. By re-evaluating published results considering the taxonomy of the studied corals and the N:P stoichiometry of their nutrient environment, we could resolve some of the major apparent contradictions. Our analysis suggests that Acroporids behave differently to several other common genera and show distinct responses to specific nutrient treatments. We hypothesised that both the concentrations of dissolved inorganic N and P in the water and their stoichiometry shape skeletal growth and microstructure. We tested this hypothesis by exposing Acropora polystoma fragments to four nutrient treatments for > 10 weeks: high nitrate/high phosphate (HNHP), high nitrate/low phosphate (HNLP), low nitrate/high phosphate (LNHP) and low nitrate/low phosphate (LNLP). HNHP corals retained high zooxanthellae densities and their linear extension and calcification rates were up to ten times higher than in the other treatments. HNLP and LNLP corals bleached through loss of symbionts. The photochemical efficiency (Fv/Fm) of residual symbionts in HNLP corals was significantly reduced, indicating P-starvation. Micro-computed tomography (µCT) of the skeletal microstructure revealed that reduced linear extension in nutrient limited or nutrient starved conditions (HNLP, LNHP, LNLP) was associated with significant thickening of skeletal elements and reduced porosity. These changes can be explained by the strongly reduced linear extension rate in combination with a smaller reduction in the calcification rate. Studies using increased skeletal density as a proxy for past thermal bleaching events should consider that such an increase in density may also be associated with temperature-independent response to the nutrient environment. Furthermore, the taxonomy of corals and seawater N:P stoichiometry should be considered when analysing and managing the impacts of nutrient pollution.
... To address this limitation, synthetic N fertilizers are applied to about 135 million Ha of agricultural land. However, these synthetic N inputs also have a range of environmental consequences including the contamination of groundwater resources , surface water contamination leading to eutrophication (Ayele and Atlabachew 2021), damage to reefs (Lapointe et al. 2019), gaseous losses contributing to acid rainfall (Penuelas et al. 2020) and greenhouse gas emissions (Puga et al. 2020). It has been reported that about 50 million tonnes of reactive N are released per year into the environment (Bodirsky et al. 2014). ...
Article
Full-text available
Globally, nitrogen (N) fertilizer demand is expected to reach 112 million tonnes to support food production for about 8 billion people. However, more than half of the N fertilizer is lost to the environment with impacts on air, water and soil quality, and biodiversity. Importantly, N loss to the environment contributes to greenhouse gas emissions and climate change. Nevertheless, where N fertilizer application is limited, severe depletion of soil fertility has become a major constraint to sustainable agriculture. To address the issues of low fertilizer N use efficiency (NUE), biochar-based N fertilizers (BBNFs) have been developed to reduce off-site loss and maximize crop N uptake. These products are generally made through physical mixing of biochar and N fertilizer or via coating chemical N fertilizers such as prilled urea with biochar. This review aims to describe the manufacturing processes of BBNFs, and to critically assess the effects of the products on soil properties, crop yield and N loss pathways. Graphical Abstract
... Since then, multiple disease outbreaks have nearly decimated the populations of many other key reef-building corals 6,7 . Moreover, there is an everincreasing risk of diseases that may further impact the stability of reef ecosystems, as the frequency and intensity of disease outbreaks are often related to rapidly increasing human-induced pressures, such as rising sea temperatures, decreased water quality, and nutrient enrichment [14][15][16][17][18] . ...
Article
Full-text available
Diseases are major drivers of the deterioration of coral reefs and are linked to major declines in coral abundance, reef functionality, and reef-related ecosystems services. An outbreak of a new disease is currently rampaging through the populations of the remaining reef-building corals across the Caribbean region. The outbreak was first reported in Florida in 2014 and reached the northern Mesoamerican Reef by summer 2018, where it spread across the ~450-km reef system in only a few months. Rapid spread was generalized across all sites and mortality rates ranged from 94% to <10% among the 21 afflicted coral species. Most species of the family Meandrinadae (maze corals) and subfamily Faviinae (brain corals) sustained losses >50%. This single event further modified the coral communities across the region by increasing the relative dominance of weedy corals and reducing reef functionality, both in terms of functional diversity and calcium carbonate production. This emergent disease is likely to become the most lethal disturbance ever recorded in the Caribbean, and it will likely result in the onset of a new functional regime where key reef-building and complex branching acroporids, an apparently unaffected genus that underwent severe population declines decades ago and retained low population levels, will once again become conspicuous structural features in reef systems with yet even lower levels of physical functionality.
... Nevertheless, compared with the DIN concentrations in overseas coral communities (DIN > 1 μM, Bell, 1992), even those corresponding to high coral cover in Hong Kong waters are considered to be eutrophic. For instance, based on the results of Lapointe et al. (2019), 20 % coral cover corresponds to a DIN of 0.64 μM in the lower Florida Keys (Data extracted by Data Graph Digitizer 2.26; http://getdata-graph-digi tizer.com). Like other coral communities in urban areas (Heery et al., 2018), the GBA coral communities may have adapted to eutrophication by shifting the community compositions to stress-tolerant genera such as Porites, Platigyra and Favites (Duprey et al., 2016), and nutrient-sensitive genera may have become rare, when compared with a study conducted in the 1980s reporting the dominance of Acropora and Montipora (Zhang and Zou, 1987). ...
Article
Coral communities in China's Great Bay Area (GBA) have experienced severe degradation, but only limited information is available about their community structure. We surveyed 20 sites across three regions (Daya Bay, Dapeng Bay, Wanshan Islands) in GBA to provide an updated baseline of these urban coral communities. Live coral cover varied substantially, with the lowest values (<2 %) found inside the highly urbanized Daya Bay, and highest values (40–47 %) from offshore islands that are less affected by human activities. The two sites with the lowest live coral cover had a high percentage of dead coral. Five groups of coral communities could be identified, with most of them characterized by dominance of massive and encrusting coral species. Both coral cover and generic richness were negatively correlated with dissolved inorganic nitrogen in the water column, indicating that nutrient pollution could potentially constrain the development of these urban coral communities.
... Global coral reef declines are accelerating with increased industrialization, urbanization and agriculture (Lapointe et al., 2019). Coral bleaching, whitening with the loss of endosymbiotic Symbiodiniaceae, occurred globally and has been recognized as the main reason for coral mortality and coral reef degradation (Hughes et al., 2017). ...
Article
The global phenomenon of coral bleaching under thermal stress has been recognized as the primary driver underlying coral reef degradation. The coral bacterial community plays an important role in the stability of coral reef ecosystem. Dimethylsulfoniopropionate (DMSP) and its associated metabolites are essential for the establishment of coral bacterial communities and provide key benefits for overall coral health and bleaching recovery. Substantial research to date has focused on the bacterial community composition, metabolism and functional properties within the coral holobiont, but less attention has been paid to the role of bacteria in seawater surrounding corals under thermal stress. Here, we investigated bacterial community composition, biological functions and DMSP metabolism changes of the seawater surrounding corals under thermal stress. We found that microbial community in seawater surrounding corals changed under thermal stress, and corals bleached eventually. The abundance of Rhodobacterales, Flavobacteriales and Rhizobiales increased while Chitinophagales and SAR11 decreased as temperature elevated. Correspondingly, stress tolerant, biofilm forming and mobile elements increased, resulting in large part from changes in Rhodobacterales and Phaeodactylibacter abundance. DMSP producing and catabolic levels in seawater surrounding corals were enhanced under thermal stress with higher dsyB (1.46-fold), dddP (2.43-fold) and dmdA (1.47-fold) detected. This study reveals the biological functions and metabolisms of bacteria in the water surrounding corals, providing valuable insight on how these communities and functions change in coral reef ecosystem under thermal stress.
Article
Concurrent rise in the prevalence of conspicuous benthic cyanobacterial mats and the incidence of coral diseases independently mark major axes of degradation of coral reefs globally. Recent advances have uncovered the potential for the existence of interactions between expanding cover of cyanobacterial mats and coral disease, especially Black Band Disease (BBD), and this intersection represents both an urgent conservation concern and critical challenge for future research. Here, we propose links between the transmission of BBD and benthic cyanobacterial mats. We synthesize molecular and ecophysiological evidence suggesting that cyanobacterial mats may create and maintain physically favorable benthic refugia for BBD pathogens while directly harboring BBD precursor assemblages, and discuss how mats may serve as direct (mediated via contact) and indirect (mediated via predator-prey-pathogen relationships) vectors for BBD pathogens. Finally, we identify and outline future priority research directions that are aligned with actionable management practices and priorities to support evidence-based coral conservation practices.
Article
Bali, Indonesia sits within the coral triangle and is internationally recognised for its high coral reef diversity. The health of Bali’s marine ecosystems has declined in recent decades, and this is thought to be due to threats from climate change, destructive fishing practices, pollution, outbreaks coral eating invertebrates, coral disease and unsustainable tourism. As a response, multiple conservation strategies have been introduced by the island’s communities, non-government organisations and governments, with the aim of preventing further decline, as well as restoring already degraded coral reefs. This literature review provides an in-depth analysis of the tools used to conserve Bali’s coral reefs, and compares them to those used in other countries. In light of international ‘best practice’ in coral reef conservation, this review makes suggestions on how Bali could better conserve its coral reef ecosystems. These include (1) increasing its designation of official Marine Protected Areas (MPAS) and strengthening management of existing ones, (2) creating an MPA network, (3) substantially reducing marine plastic pollution, (4) continuing artificial reef construction in degraded habitats, (5) continuing to develop Bali as an ecotourism destination, (6) increasing engagement in global science to inform marine conservation decision-making, and (7) developing more marine monitoring programmes.
Article
Full-text available
The global‐scale degradation of coral reefs has reached a critical threshold wherein further declines threaten both ecological functionality and the persistence of reef structure. Geological records can provide valuable insights into the long‐term controls on reef development that may be key to solving the modern coral‐reef crisis. Our analyses of new and existing coral‐reef cores from throughout the Florida Keys reef tract (FKRT) revealed significant spatial and temporal variability in reef development during the Holocene. Whereas maximum Holocene reef thickness in the Dry Tortugas was comparable to elsewhere in the western Atlantic, most of Florida's reefs had relatively thin accumulations of Holocene reef framework. During periods of active reef development, average reef accretion rates were similar throughout the FKRT at ~3 m/ky. The spatial variability in reef thickness was instead driven by differences in the duration of reef development. Reef accretion declined significantly from ~6,000 years ago to present, and by ~3,000 years ago, the majority of the FKRT was geologically senescent. Although sea level influenced the development of Florida's reefs, it was not the ultimate driver of reef demise. Instead, we demonstrate that the timing of reef senescence was modulated by subregional hydrographic variability, and hypothesize that climatic cooling was the ultimate cause of reef shutdown. The senescence of the FKRT left the ecosystem balanced at a delicate tipping point at which a veneer of living coral was the only barrier to reef erosion. Modern climate change and other anthropogenic disturbances have now pushed many reefs past that critical threshold and into a novel ecosystem state, in which reef structures built over millennia could soon be lost. The dominant role of climate in the development of the FKRT over timescales of decades to millennia highlights the potential vulnerability of both geological and ecological reef processes to anthropogenic climate change.
Article
Full-text available
Lake Okeechobee, FL, USA, has been subjected to intensifying cyanobacterial blooms that can spread to the adjacent St. Lucie River and Estuary via natural and anthropogenically-induced flooding events. In July 2016, a large, toxic cyanobacterial bloom occurred in Lake Okeechobee and throughout the St. Lucie River and Estuary, leading Florida to declare a state of emergency. This study reports on measurements and nutrient amendment experiments performed in this freshwater-estuarine ecosystem (salinity 0–25 PSU) during and after the bloom. In July, all sites along the bloom exhibited dissolved inorganic nitrogen-to-phosphorus ratios < 6, while Microcystis dominated (> 95%) phytoplankton inventories from the lake to the central part of the estuary. Chlorophyll a and microcystin concentrations peaked (100 and 34 μg L⁻¹, respectively) within Lake Okeechobee and decreased eastwards. Metagenomic analyses indicated that genes associated with the production of microcystin (mcyE) and the algal neurotoxin saxitoxin (sxtA) originated from Microcystis and multiple diazotrophic genera, respectively. There were highly significant correlations between levels of total nitrogen, microcystin, and microcystin synthesis gene abundance across all surveyed sites (p < 0.001), suggesting high levels of nitrogen supported the production of microcystin during this event. Consistent with this, experiments performed with low salinity water from the St. Lucie River during the event indicated that algal biomass was nitrogen-limited. In the fall, densities of Microcystis and concentrations of microcystin were significantly lower, green algae co-dominated with cyanobacteria, and multiple algal groups displayed nitrogen-limitation. These results indicate that monitoring and regulatory strategies in Lake Okeechobee and the St. Lucie River and Estuary should consider managing loads of nitrogen to control future algal and microcystin-producing cyanobacterial blooms.
Article
Full-text available
Nutrient pollution can increase the prevalence and severity of coral disease and bleaching in ambient temperature conditions or during experimental thermal challenge. However, there have been few opportunities to study the effects of nutrient pollution during natural thermal anomalies. Here we present results from an experiment conducted during the 2014 bleaching event in the Florida Keys, USA, that exposed Agaricia sp. (Undaria) and Siderastrea siderea corals to 3 types of elevated nutrients: nitrogen alone, phosphorous alone, and the combination of nitrogen and phosphorus. Overall, bleaching prevalence and severity was high regardless of treatment, but nitrogen enrichment alone both prolonged bleaching and increased coral mortality in Agaricia corals. At the same time, the elevated temperatures increased the prevalence of Dark Spot Syndrome (DSS), a disease typically associated with cold temperatures in Siderastrea siderea corals. However, nutrient exposure alone did not increase the prevalence or severity of disease, suggesting that thermal stress overwhelms the effects of nutrient pollution on this disease during such an extreme thermal event. Analysis of 78 Siderastrea siderea microbial metagenomes also showed that the thermal event was correlated with significant shifts in the composition and function of the associated microbiomes, and corals with DSS had microbiomes distinct from apparently healthy corals. In particular, we identified shifts in viral, archaeal, and fungal families. These shifts were likely driven by the extreme temperatures or other environmental co-variates occurring during the 2014 bleaching event. However, no microbial taxa were correlated with signs of DSS. Furthermore, although nutrient exposure did not affect microbial alpha diversity, it did significantly affect microbiome beta-diversity, an effect that was independent of time. These results suggest that strong thermal anomalies and local nutrient pollution both interact and act independently to alter coral health in a variety of ways, that ultimately contribute to disease, bleaching, and mortality of reefs in the Florida Keys.
Article
Full-text available
Nutrient enrichment is a significant global-scale driver of change in coastal waters, contributing to an array of problems in coastal ecosystems. The St. Lucie Estuary (SLE) in southeast Florida has received national attention as a result of its poor water quality (elevated nutrient concentrations and fecal bacteria counts), recurring toxic Microcystis aeruginosa blooms, and its proximity to the northern boundary of tropical coral species in the United States. The SLE has an artificially large watershed comprised of a network of drainage canals, one of which (C-44) is used to lower the water level in Lake Okeechobee. Public attention has primarily been directed at nutrient inputs originating from the lake, but recent concern over the importance of local watershed impacts prompted a one-year watershed study designed to investigate the interactions between on-site sewage treatment and disposal systems (OSTDS or septic systems), groundwaters, and surface waters in the SLE and nearshore reefs. Results provided multiple lines of evidence of OSTDS contamination of the SLE and its watershed: 1) dissolved nutrients in groundwaters and surface waters were most concentrated adjacent to two older (pre-1978) residential communities and the primary canals, and 2) sucralose was present in groundwater at residential sites (up to 32.0 mg/L) and adjacent surface waters (up to 5.5 mg/L), and 3) d 15 N values in surface water (+7.5 o / oo), macroalgae (+4.4 o / oo) and phytoplankton (+5.0 o / oo) were within the published range (>+3 o / oo) for sewage N and similar to values in OSTDS-contaminated groundwaters. Measured d 15 N values in M. aeruginosa became increasingly enriched during transport from the C-44 canal (5.8 o / oo) into the mid-estuary (8.0 o / oo), indicating uptake and growth on sewage N sources within the urbanized estuary. Consequently, there is a need to reduce N and P loading, as well as fecal loading, from the SLE watershed via septic-to-sewer conversion projects and to minimize the frequency and intensity of the releases from Lake Okeechobee to the SLE via additional water storage north of the lake. These enhancements would improve water quality in both the SLE and Lake Okeechobee, reduce the occurrence of toxic harmful algal blooms in the linked systems, and improve overall ecosystem health in the SLE and downstream reefs.
Article
Full-text available
Coral reefs are degrading to algae-dominated reefs worldwide, with alterations of coral microbiomes commonly co-occurring with reef demise. The severe thermal anomaly during the 2016 El Niño event in the South Pacific killed many corals and stressed others. We examined the microbiome of turf algae and of the coral Porites sp. in contact with turf during this thermal event to investigate algal turf effects on the coral microbiome during a period of environmental stress. The microbial composition of turf did not differ between coral-contacted and non-contacted turfs. However, microbiomes of corals in direct contact with turf were similar to those of the turf microbiome, but differed significantly from coral portions 5 cm from the point of turf/coral contact and from portions of the coral that looked most healthy, regardless of location. Although the majority of significant differences occurred in coral samples at the point of contact, a small subset of microbial taxa was enriched in coral tissues taken 5 cm from turf contact compared to all other sample types, including samples from areas of the coral that appeared most healthy. These results suggest that the coral microbiome is susceptible to colonization by microbes from turf, but not vice versa. Results also suggest that algal contact elicits a subtle shift in the coral microbiome just beyond the contact site. The combination of turf microbiome stability and coral microbiome vulnerability at areas of contact may contribute to the continued decline in coral cover and increase in algal cover associated with coral–algae phase shifts.
Article
Deriving inherent optical properties (IOPs) and other water quality parameters from satellite remote sensing data covering optically shallow environments has historically been problematic due to difficulties in separating the benthic signal from that of the water column. While recent advances have improved such retrievals, most methods have high uncertainties for very shallow (< 5 m) or very bright (e.g., carbonate sand) targets. Here, we present a two-stage process to improve IOP derivations from satellite-derived reflectance data, termed the Shallow Water Optimization with Resolved Depth (SWORD). Within this process, a raster bathymetry is first derived through multiple pixel-wise implementations of a spectral matching algorithm on mapped reflectance data. This bathymetry is then used as a fixed input in subsequent implementations of the algorithm, leading to improved IOP retrievals. The SWORD approach was developed and tested using a dataset of simulated reflectance spectra as well as MERIS reflectance data covering two optically shallow water environments. Bathymetries derived using this process showed strong agreement with those determined from soundings and coastal relief models. Although SWORD-derived raster albedo maps showed general concordance to benthic habitat surveys, we found limited benefit of fixing this parameter in spectral matching routines. IOP derivations from SWORD show expected spatiotemporal patterns in the Florida Keys region, consistent with local hydrodynamic processes, seasonal fluctuations, and known anomalous events. This approach is portable to multispectral reflectance data from similar satellite instruments, allowing regular and ongoing assessment and monitoring of optical water quality for ecologically and economically important marine systems.
Article
A new online resource from the National Oceanic and Atmospheric Administration provides an interactive view of global satellite ocean color and true-color imagery.
Article
Shifts in competitive balance between key functional groups may drive regime shifts in tropical and temperate marine ecosystems. On shallow reefs, regime shifts increasingly involve changes from spatial dominance by foundation species (e.g. reefbuilding corals, canopy-forming algae) to dominance by turf-forming algae differing in structural complexity. To disentangle competitive inter actions fromother processes that may contribute to these shifts, we conducted a global meta-analysis of manipulative competition experiments between foundation and turf-forming species. Canopy- forming algae had consistently negative effects on abundance of turfforming algae, particularly on subtidal reefs, but with a tendency towards larger effects on delicate filamentous forms compared to articulated coralline and corticated/coarsely branching turf. Competitive effects of turf-forming algae on canopy species were limited to early life-history stages, and similarly varied between turf functional groups and between subtidal and intertidal reefs. Conversely, shorter filamentous turf assemblages typical of tropical reefs had no significant effect on settlement and survival of coral larvae. Interactions between turf-forming algae and established coral colonies were negative overall, but variable in magnitude. Mean effect sizes indicated that corals suppress turf abundance, but not vice versa. However, turf-forming algae significantly im - pacted coral growth and tissue mortality. We suggest reefs with extensive cover of foundation species are resistant to proliferation of turf algae, but competition will inhibit recovery of reefs following disturbances that enable turf algae to establish. Therefore, competitive effects of foundation and turf-forming species must be accounted for to effectively evaluate the stability of these undesirable regime shifts and recovery potential under alternative climate and management scenarios.
Article
Australia's Great Barrier Reef (GBR) is under pressure from a suite of stressors including cyclones, crown-of-thorns starfish (COTS), nutrients from river run-off and warming events that drive mass coral bleaching. Two key questions are: how vulnerable will the GBR be to future environmental scenarios, and to what extent can local management actions lower vulnerability in the face of climate change? To address these questions, we use a simple empirical and mechanistic coral model to explore six scenarios that represent plausible combinations of climate change projections (from four Representative Concentration Pathways, RCPs), cyclones and local stressors. Projections (2017–2050) indicate significant potential for coral recovery in the near-term, relative to current state, followed by climate-driven decline. Under a scenario of unmitigated emissions (RCP8.5) and business-as-usual management of local stressors, mean coral cover on the GBR is predicted to recover over the next decade and then rapidly decline to only 3% by year 2050. In contrast, a scenario of strong carbon mitigation (RCP2.6) and improved water quality, predicts significant coral recovery over the next two decades, followed by a relatively modest climate-driven decline that sustained coral cover above 26% by 2050. In an analysis of the impacts of cumulative stressors on coral cover relative to potential coral cover in the absence of such impacts, we found that GBR-wide reef performance will decline 27%–74% depending on the scenario. Up to 66% of performance loss is attributable to local stressors. The potential for management to reduce vulnerability, measured here as the mean number of years coral cover can be kept above 30%, is spatially variable. Management strategies that alleviate cumulative impacts have the potential to reduce the vulnerability of some midshelf reefs in the central GBR by 83%, but only if combined with strong mitigation of carbon emissions.
Article
Eutrophication, or excessive nutrient enrichment, threatens water resources across the globe. We show that climate change–induced precipitation changes alone will substantially increase (19 ± 14%) riverine total nitrogen loading within the continental United States by the end of the century for the “business-as-usual” scenario. The impacts, driven by projected increases in both total and extreme precipitation, will be especially strong for the Northeast and the corn belt of the United States. Offsetting this increase would require a 33 ± 24% reduction in nitrogen inputs, representing a massive management challenge. Globally, changes in precipitation are especially likely to also exacerbate eutrophication in India, China, and Southeast Asia. It is therefore imperative that water quality management strategies account for the impact of projected future changes in precipitation on nitrogen loading.