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 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

Feeding Ecology of Dolphinfish in the Western Gulf of Mexico

Dolphinfish Coryphaena hippurus support important commercial and recreational fisheries in the Gulf of Mexico. Understanding the feeding ecology of this economically important pelagic fish is key to its sustainable management; however, dietary data from this region are sparse. We conducted a comprehensive diet study to develop new trophic baselines and investigate potential ontogenetic and sex-related shifts in Dolphinfish feeding ecology. The stomach contents of 357 Dolphinfish (27.6–148.5 cm TL) were visually examined from fishery-dependent sources off Port Aransas, Texas. Our analyses revealed a highly piscivorous diet with Actinopterygii comprising 70.44% of the stomach contents by number. The most commonly observed taxa were carangid (12.45%N) and tetraodontiform (12.08%N; families Balistidae, Monacanthidae, and Tetraodontidae) fishes. Malacostracans were also common (24.83%N), mostly in the form of pelagic megalopae. Other prey categories included squid and the critically endangered Kemp’s Ridley sea turtles Lepidochelys kempii. Although increasingly commom in larger fish, Sargassum spp. was found across a range of sizes in Dolphinfish, indicating that these fish feed from this drifting macroalgae throughout ontogeny. An ontogenetic shift from primary consumption of carangids and brachyurans in smaller size-classes to tetraodontids, monocanthids, and squid in larger size-classes was also observed. No sex-related difference in diet was observed. The overall infection rate for gastric parasites was 54%, an order of magnitude increase from that previously reported in the region, but consistent with recent studies from other areas. Trematode parasites in the genus Dinurus were found in 55% of stomachs and nematode parasites of the family Raphidascarididae in 16% of stomachs. Overall, Dolphinfish in the western Gulf of Mexico are highly opportunistic carnivores with a gastrointestinal parasite burden consistent with that reported in other ocean basins. These data will be important for sustainable management of this economically important species

On the Atlantic Pelagic \u3c/i\u3eSargassum\u3c/i\u3e\u27s Role In Carbon Fixation and Sequestration

The extensive blooms of the pelagic Sargassum in the Atlantic raised the question of whether this brown seaweed may play an important role in climate change mitigation through carbon fixation and carbon sequestration, as argued in several recent papers. Using simple calculations and published values on Sargassum coverage, biomass density, carbon/biomass ratio, primary productivity, and carbon sequestration efficiency, we show that the total carbon stock in pelagic Sargassum of the entire Atlantic, even during the peak month, is unlikely to exceed 3.61 × 10−3 Pg C, and carbon fixation cannot exceed 6.0 million tons C month−1. While the carbon fixation estimate represents an upper bound, it is still Sargassum appears significant locally within the Atlantic Sargassum belt. The analysis further suggests that, while the Atlantic pelagic Sargassum may play an important role in affecting local carbon budget and carbon sequestration, its contribution to either carbon stock or carbon sequestration at a global scale may be insignificant. This, however, does not diminish the importance of Atlantic pelagic Sargassum in many other aspects

Impacts of the Deepwater Horizon Oil Spill On the Reproductive Biology of Spotted Seatrout (\u3ci\u3eCynoscion nebulosus\u3c/i\u3e)

The April 2010 Deepwater Horizon (DWH) oil spill released an estimated 4.1 million barrels of crude oil as well as 2.1 million gallons of the dispersant Corexit 9500 into the northern Gulf of Mexico (GOM). The marshes and coastal shorelines along the north central GOM were impacted as crude and dispersed oil from the offshore blowout moved onshore. Although Louisiana waters received the heaviest impacts of bioavailable polycyclic aromatic compounds (PAHs) immediately after the spill, Mississippi coastal areas were also significantly impacted (Allan et al. 2012). Although the amount of measured PAHs in coastal waters in Mississippi decreased to prespill levels by August 2010, PAH levels did not return to prespill levels in Louisiana waters until March 2011 (Allan et al. 2012). Despite these impacts, juvenile fish communities in Louisiana and Mississippi seagrass meadows did not show a dramatic decline in 2010 collections compared with historical (2006–2009) collections (Fodrie and Heck 2011), suggesting fish that were spawned during the oil spill were more resilient than expected. However, sublethal effects of oil exposure on adult fishes may alter reproductive capacity, resulting in future impacts on fish populations. For instance, PAHs are known to have a deleterious effect on vitellogenesis (the production of egg-yolk proteins) in fishes, which can substantially reduce ovarian development and reproductive output (Nicholas 1999). Laboratory exposure of Atlantic croaker (Micropogonias undulatus) to diesel fuel oil impaired ovarian growth and oocyte development (Thomas and Budiantara 1995), while wild-caught yellowfin sole (Limanada aspera) and Dolly Varden (Salevelinus malma) exhibited reproductive impairment for several years after the Exxon Valdez oil spill (Sol et al. 2000). Examining the reproductive biology of GOM fishes affected by the DWH oil spill is a first step in helping to determine potential long-term population impacts of the oil spill

Nitrogen Enrichment, Altered Stoichiometry, and Coral Reef Decline at Looe Key, Florida Keys, USA: a 3-decade Study

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

Sound Science, not Politics, must Inform Restoration of Florida Bay and the Coral Reefs of the Florida Keys

The comment by Julian (2020) criticizes aspects of our paper, “Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA.” The comment begins by misrepresenting our extensive literature review, while providing no justification for the claim of a “skewed reading.” Julian’s critique focused on methods of data handling, statistics, and spatial awareness, which we demonstrate in every case to be either irrelevant or incorrect. We provide additional supporting data that refute these claims. For example, Julian criticized the removal of data points below the method detection limits (MDLs), but when these points are included, the results do not change. Further, Julian criticized our removal of outliers, but so few points were excluded that it did not change the results of the statistical analyses. Julian also misinterpreted the methods of our correlation and stepwise regression analyses but did not dispute the Kruskal–Wallis tests of our 30-year dataset that revealed significant decadal changes. Julian’s closing paragraph is replete with misinformation and demonstrates a lack of understanding as to how increased freshwater flows associated with Everglades Restoration have led to a worsening of algal blooms and coral decline in the Florida Keys National Marine Sanctuary (FKNMS). This comment represents a smokescreen to confuse the scientific community about the physical connectivity of the Everglades basin and the FKNMS. Past water management policies based on politics, not sound science, have caused irreparable and ongoing environmental damage to sensitive coral reef communities in the FKNMS

Trophic ecology of red snapper Lutjanus campechanus on natural and artificial reefs: interactions between annual variability, habitat, and ontogeny

In the Gulf of Mexico (GOM), oil and gas platforms have created an expansive network of artificial reefs. Generally, policies mandate removal of these structures post-production; however, many enter ‘Rigs-to-Reefs’ (RTR) programs that convert the rig materials into artificial reefs (‘reefing’). Despite the growth of RTR programs worldwide, the functionality of the resulting habitats remains uncertain, particularly due to the lack of comparative studies with natural systems. To address this data gap as it relates to trophic ecology, we compared annual, ontogenetic, and habitat-specific diet and stable isotope signatures (δ13C and δ15N) of adult red snapper Lutja - nus campe chanus (n = 1585) from relic coralgal natural reefs to those of fish from standing and reefed platforms located in similar depth strata of the northwestern GOM. Stomach content analyses revealed significant effects of year, habitat, and total length on prey composition. Subsequent analyses of stable isotope values by size class identified a non-linear relationship with ontogeny. δ13C and δ15N values at reefed platforms and natural reefs decreased in the medium size class (401− 600 mm total length), whereas fish from standing platforms exhibited more consistent feeding patterns across ontogeny. Annual variability was also observed in δ13C and δ15N values, with 2013 and 2014 significantly different from 2015. These findings suggest that the trophic impacts of habitat type on reef fishes are more complex than previously considered in the GOM and that reefed platforms provide foraging opportunities more similar to natural reefs than standing platforms