Chasing Nutrients and Algal Blooms in Gulf and Caribbean Waters: A Personal Story

Over the past 5 decades, coastal waters have experienced unprecedented global change, including widespread eutrophication, harmful algal blooms (HAB), dead zones, and loss of biodiversity. During this period, I have studied the effects of nutrients (N, P) on HAB dynamics in tropical seagrass and coral reef ecosystems. Important findings that emerged from my research include: 1) a primary role of anthropogenic nitrogen (N) relative to phosphorus (P) as a driving factor in algal blooms and coastal eutrophication; 2) altered N:P stoichiometry that results in greater P—limitation and metabolic stress in reef corals; 3) recognition that macroalgal blooms be considered as a type of HAB because of their increasingly negative impacts on oceans and human health; and 4) mitigation of anthropogenic N inputs can increase resiliency of seagrass and coral reef ecosystems relative to population growth and climate change. Major developments during the research involved the use of computers and software; EAN NITROX, dive computers, and high resolution underwater video to make SCUBA surveys safer and more effective; analysis of stable nitrogen isotopes, sucralose, and other human tracers to discriminate between natural and anthropogenic N sources; and satellite remote sensing to better monitor the large—scale HAB phenomena. My research sparked considerable debate about the root cause(s) of algal blooms on Caribbean coral reefs, as several senior coral reef biologists had concluded this problem was caused solely by the reduction of reef grazers. Since 2011, the massive Sargassum influx to the Caribbean region appears to be a eutrophication response to increasing nutrients in the tropical Atlantic Ocean and is now considered the largest HAB on the planet. Going forward, early career scientists need to extend research on declining coastal ecosystem health to upland watersheds to better understand and mitigate nutrient pollution at its source(s) to enhance resilience of seagrass and coral reef ecosystems to climate change

Nutrient content and stoichiometry of pelagic Sargassum reflects increasing nitrogen availability in the Atlantic Basin

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Lapointe, B. E., Brewton, R. A., Herren, L. W., Wang, M., Hu, C., McGillicuddy, D. J., Lindell, S., Hernandez, F. J., & Morton, P. L. Nutrient content and stoichiometry of pelagic Sargassum reflects increasing nitrogen availability in the Atlantic Basin. Nature Communications, 12(1), (2021): 3060, https://doi.org/10.1038/s41467-021-23135-7.The pelagic brown macroalgae Sargassum spp. have grown for centuries in oligotrophic waters of the North Atlantic Ocean supported by natural nutrient sources, such as excretions from associated fishes and invertebrates, upwelling, and N2 fixation. Using a unique historical baseline, we show that since the 1980s the tissue %N of Sargassum spp. has increased by 35%, while %P has decreased by 44%, resulting in a 111% increase in the N:P ratio (13:1 to 28:1) and increased P limitation. The highest %N and δ15N values occurred in coastal waters influenced by N-rich terrestrial runoff, while lower C:N and C:P ratios occurred in winter and spring during peak river discharges. These findings suggest that increased N availability is supporting blooms of Sargassum and turning a critical nursery habitat into harmful algal blooms with catastrophic impacts on coastal ecosystems, economies, and human health.This work was funded by the US NASA Ocean Biology and Biogeochemistry Program (80NSSC20M0264, NNX16AR74G) and Ecological Forecast Program (NNX17AF57G), NOAA RESTORE Science Program (NA17NOS4510099), National Science Foundation (NSF-OCE 85–15492 and OCE 88–12055), “Save Our Seas” Specialty License Plate funds, granted through the Harbor Branch Oceanographic Institute Foundation, Ft. Pierce, FL, and a Red Wright Fellowship from the Bermuda Biological Station. A portion of this work was performed at the National High Magnetic Field Laboratory, which is supported by National Science Foundation Cooperative Agreement No. DMR-1644779 and the State of Florida. D.J.M. gratefully acknowledges the Holger W. Jannasch and Columbus O’Donnell Iselin Shared Chairs for Excellence in Oceanography, as well as support from the Mill Reef Fund

The State of Coral Reef Ecosystems of Southeast Florida

The northern extension of the Florida reef tract and a complex of limestone ridges run parallel to the subtropical Atlantic coastline of southeast Florida. Spanning 170 km from the northern border of Biscayne National Park (BNP) in Miami-Dade County to the St. Lucie Inlet in Martin County, the reefs and hardbottom areas in this region support a rich and diverse biological community (Figure 5.1). Nearshore reef habitats in southeast Florida include hardbottom areas, patch reefs and worm reefs (Phragmatopoma spp.) exhibiting abundant octocoral, macroalgae, stony coral and sponge assemblages. Offshore, coral reef associated biotic assemblages occur on linear Holocene Acropora palmata mid-shelf and shelf margin reefs that extend from Miami Dade County to Palm Beach County (Lighty, 1977; Figure 5.2). Anastasia Formation limestone ridges and terraces colonized by reef biota characterize the reefs from Palm Beach County to Martin County (Cooke and Mossom, 1929). The coastal region of southeast Florida is highly developed, containing one third of Florida’s population of 16 million people (U.S. Census Bureau, 2006). Many southeast Florida reefs are located just 1.5 km from this urbanized shoreline. Despite their unique position as the highest latitude reefs along the western Atlantic seaboard, the reefs of southeast Florida have only recently received limited scientific and resource management attention. Andrews et al. (2005) discussed the reefs of southeast Florida and the critical need to implement actions that fill resource knowledge gaps and address conservation and threats to reef health. This report further examines and updates the list of stressors imperiling the health of southeast Florida’s reefs, and presents information gained from new research, monitoring and management efforts to determine the extent and condition of reef resources in this distinctive region

A Tissue Biomarker Panel Predicting Systemic Progression after PSA Recurrence Post-Definitive Prostate Cancer Therapy

Many men develop a rising PSA after initial therapy for prostate cancer. While some of these men will develop a local or metastatic recurrence that warrants further therapy, others will have no evidence of disease progression. We hypothesized that an expression biomarker panel can predict which men with a rising PSA would benefit from further therapy.A case-control design was used to test the association of gene expression with outcome. Systemic (SYS) progression cases were men post-prostatectomy who developed systemic progression within 5 years after PSA recurrence. PSA progression controls were matched men post-prostatectomy with PSA recurrence but no evidence of clinical progression within 5 years. Using expression arrays optimized for paraffin-embedded tissue RNA, 1021 cancer-related genes were evaluated-including 570 genes implicated in prostate cancer progression. Genes from 8 previously reported marker panels were included. A systemic progression model containing 17 genes was developed. This model generated an AUC of 0.88 (95% CI: 0.84-0.92). Similar AUCs were generated using 3 previously reported panels. In secondary analyses, the model predicted the endpoints of prostate cancer death (in SYS cases) and systemic progression beyond 5 years (in PSA controls) with hazard ratios 2.5 and 4.7, respectively (log-rank p-values of 0.0007 and 0.0005). Genes mapped to 8q24 were significantly enriched in the model.Specific gene expression patterns are significantly associated with systemic progression after PSA recurrence. The measurement of gene expression pattern may be useful for determining which men may benefit from additional therapy after PSA recurrence

The green macroalga Caulerpa prolifera replaces seagrass in a nitrogen enriched, phosphorus limited, urbanized estuary

The Indian River Lagoon (IRL) on Florida’s east-central coast is a highly developed eutrophic estuary, experiencing harmful algal blooms (HABs). Beginning in 2011, the IRL experienced multiple phytoplankton HABs that were followed by widespread seagrass losses and expanding blooms of the rhizophytic macroalga Caulerpa prolifera. To better understand factors related to the changing benthic cover, long-term monitoring data spanning 2011–2020 for seagrass and C. prolifera percent cover at six locations in the northern IRL and Banana River Lagoon were considered in multivariate analyses with environmental parameters (temperature, salinity, pH, dissolved oxygen, etc.), dissolved nutrient and chlorophyll-a concentrations, and macroalgal carbon (δ13C) and nitrogen (δ15N) stable isotopes, elemental composition (%C, %N, %P), and nutrient ratios (C:N:P). Data reduction using the global Bio-Env + STepwise (BEST) procedure followed by linkage tree (LINKTREE) analyses indicated the variable most correlated to annual differences in benthic cover was macroalgal C:P. Following seagrass losses, P availability increased, as the result of heavy rainfall, increased sediment flux, and/or more bioavailable P due to seagrass losses. The most correlated variables among differences in location were C:P, δ13C, and salinity, which could be related to less urbanization at the northernmost sites that had lower percent cover of C. prolifera. While not identified as a significant variable, the increase in C. prolifera was associated with four years (2016–2019) of high ammonium concentrations (6.26 µM) and macroalgal δ15N values (+8.67 ‰), linking the blooms to the influence of human waste. The variables identified in this work as related to benthic cover suggest that reducing stormwater runoff and inputs of human waste will promote the recovery of seagrasses in the IRL. These findings have implications for urbanized estuaries experiencing seagrass loss globally

Winter Nutrient Pulse and Seagrass Epiphyte Bloom: Evidence of Anthropogenic Enrichment or Natural Fluctuations in the Lower Florida Keys?

Nutrient enrichment continues to disrupt marine ecosystem function worldwide. Assessing eutrophication in seagrass ecosystems such as the Great White Heron National Wildlife Refuge (GWHNWR), Florida Keys is critical for protecting the diverse community that depends on the intertidal and subtidal seagrass beds. We quantified water column nutrients, chlorophyll a, tissue nutrients in macroalgae and Thalassia testudinum, and epiphyte percent cover on seagrasses on tidal flats seasonally over 1 year at three sites: Howe Key, Water Keys, and Upper Harbor Key. Water column nutrients (total nitrogen, total phosphorus, nitrate–nitrite, ammonium, dissolved inorganic nitrogen, dissolved organic nitrogen, soluble reactive phosphorus, dissolved organic phosphorus) increased from fall to winter at Water Keys. These increased nutrients coincided with a bloom of the epiphyte Spyridia filamentosa on seagrasses that exceeded 40 % cover at Water Keys and Upper Harbor Key in two consecutive seasons. Seagrasses at all sites had chronic percent cover of small epiphytes exceeding 60 %. Additionally, low δ13C in T. testudinum tissues at Upper Harbor Key compared to the other sites suggested variations in carbon sources across the study area. Spatial patterns in macrophyte nitrogen-tophosphorus (N:P) ratios point to sources of nutrients from the inhabited islands of the Keys and from the Gulf of Mexico. Water column total nitrogen and total phosphorus concentrations exceeded the numeric nutrient criteria for the study area suggesting that the area should be monitored closely

Relative effects of physical and small-scale nutrient factors on the distribution of tropical seagrasses in the Great White Heron National Wildlife Refuge, Lower Florida Keys

We tested the relative effects of physical factors such as exposure time and water depth as well as nutrient availability on Thalassia testudinum, Halodule wrightii and Syringodium filiforme distribution within the Great White Heron National Wildlife Refuge, Florida Keys. We quantified the percent cover of each sea- grass species in 1-m2 plots (n = 325) along intertidal and shallow subtidal flats adjacent to Upper Harbor Key Water Keys and Howe Key. We used model selection to evaluate the effects of physical parameters and water column nutrients on the percent cover and composition of seagrass species within plots. Best models were selected based on lowest Akaike’s information criteria (AIC) values and maximum model weights (ωi). We found that the presence of the other species, distance to nearest island and time of exposure during diurnal low tides best explained the distribution of T. testudinum (ωi = 0.44). Model averaged parameter estimates (ˇ) showed that H. wrightii and S. filiforme had the greatest negative influence on T. testudinum (ˇ = −0.396, −0.278, respectively). H. wrightii distribution was affected strongly by the presence of the other species, distance to Pine Channel, exposure time and mean lower low water (MLLW) (ωi = 0.56) with T. testudinum and S. filiforme exerting the greatest negative influences (ˇ = −0.450, −0.184, respectively). The best model indicated that S. filiforme was strongly influenced by the other species, distance to Pine Channel and MLLW (ωi = 0.5). Model averaging indicated that S. filiforme was associated with deep water (ˇMLLW = −28.0.018). Our study showcased that small scale (<100 m) habitat heterogeneity influenced the composition of seagrass communities

Evidence of large-scale chronic eutrophication in the Great Barrier Reef: quantification of chlorophyll a thresholds for sustaining coral reef communities

Long-term monitoring data show that hard coral cover on the Great Barrier Reef (GBR) has reduced by >70 % over the past century. Although authorities and many marine scientists were in denial for many years, it is now widely accepted that this reduction is largely attributable to the chronic state of eutrophication that exists throughout most of the GBR. Some reefs in the far northern GBR where the annual mean chlorophyll a (Chl a) is in the lower range of the proposed Eutrophication Threshold Concentration for Chl a (~0.2-0.3 mg m⁻³) show little or no evidence of degradation over the past century. However, the available evidence suggests that coral diseases and the crown-of-thorns starfish will proliferate in such waters and hence the mandated eutrophication Trigger values for Chl a (~0.4-0.45 mg m⁻³) will need to be decreased to ~0.2 mg m⁻³ for sustaining coral reef communities