EC #29 - Bacterial Nitrogen Levels Soar in Head

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EC #29 - Bacterial Nitrogen Levels Soar In Heat
Many Nitrogen Studies May Not Include Compost Sapropel As A Possible Nitrogen Source
The Bacteria-Nitrogen Series on The Blue Crab Forum TM
Environment Conservation Thread
Thank you, The Blue Crab Forum TM Managers for posting these Habitat and Bacteria Nitrogen newsletters – over 200,000 views to date
June 2021 revised to February 2023
This is a delayed report – February, 2015
Tim Visel retired from The Sound School June 30, 2022
Viewpoint of Tim Visel – no other agency or organization
(This paper, in draft form since 2015, was revised in 2021. Since that time, many nitrogen models have been modified for sulfur bacterial composting – T. Visel)

Nitrogen/Eelgrass TMDL Levels

Statement of Problem - While many US communities have spent hundreds of millions to remove water borne human nitrogen for increasing oxygen levels for seafood and based on TMDL nitrogen allowances it appears in some cases only a part of the many nitrogen sources were included (See EC #9, December 1, 2015 and EC #5, January 12, 2015). A significant negative nitrogen habitat factor was from leaf and natural organic material in sediments.1  This includes the bacterial discharge of nitrogen compounds (See EC #8, October 30, 2015), especially ammonia in warm seawater.  This bacterial source of nitrogen is from marine compost deposits – organic matter, mostly dead plant tissue.  This composting aspect becomes more important in warming seawater.  Warmer seawater causes rapid bacteria growths living on dead plant tissue.  Bacteria can act as a nitrogen pump from natural composting.  This compost can accumulate in low energy habitats (often tidally restricted), producing a sulfide-rich organic ooze.  It is deadly to shellfish and may contain large amounts of sulfide (See Appendix #1).

This aspect of human nitrogen removal, a large public policy concern and deserving of our attention (as any pollution impact), was introduced to the concerned public during a pronounced period of increasing heat.  The 1980's saw progressively mild or "short" winters while lengthening very hot summers.  This tended to "bank" temperature in Long Island Sound seawater, and just a few degrees could make a huge difference.  Falls ended with warmer Long Island Sound waters and if winters were mild started the spring with a few degrees "head start" for the summer heat waves.  Over time, Long Island Sound waters gradually warmed as they did a century before in the 1890's.  The largest public impact was the decline in cool water species observed or caught along the coast.  Boaters and fishers also observed these changes and reported them, such as fish kills or brown waters.  The brown waters algal blooms thrived on high ammonia levels when seawater temperatures are very warm.

The heat had an impact that was not as noticeable, a change in bacteria species that live in certain temperature ranges.  Some bacteria prefer cooler temperatures and some thrive in heat – they are called the thermophiles.  Bacteria that thrive in heat can use sulfate, a dissolved sulfur-oxygen compound in seawater as a source of oxygen.  These strains are often termed sulfate reducing bacteria or simply "SRB."  These bacterial strains have been studied since the 1920's and related impacts of sulfide release by utilizing sulfate as a source of composting oxygen (not in the elemental form).  By using sulfate as an oxygen source, their byproduct is hydrogen sulfide H2S.

As bacterial populations respond to heat, the cooler bacteria die out while the sulfate bacteria increase the production of sulfides as well as a natural waste or byproduct of sulfate metabolism. This impact was recorded (reported) in hot spells by coastal residents as bad smells emanating from coastal marshes and bays.  In reviews of the shellfish and finfish historical literature, these high sulfide events are noted as the "smell of rotting eggs," a carryover phrase from the previous hot term of the 1890's.  At this time, hidden eggs or missed eggs spoiled quickly in high heat; cracking one releases a high sulfide gas – a stink or smell.  (Cookbooks even into the 1940's – a cooler period – still advised opening eggs first into a separate bowl before adding them to a recipe.)  Many fish kills and shellfish die-offs are often preceeded by the "smell of rotting eggs," especially after a long August heat wave with little rain or wind.  High heat bacterial composting releases huge amounts of nitrogen compounds in the form of ammonia.  The farm community had long known that sealed wet, terrestrial composts leaked (or "wasted") ammonia.  The 1880 Annual Report of the Maine Board of Agriculture transmittal of January 19, 1881 on page 71 contains the following segment by W. H. Jordan, Instructor in Agriculture at the Maine State College in a much larger section titled Principles of Manuring – (my comments, T. Visel):

"Some suggestions with reference to the differences of treatment demanded by the manure from the different farm animals, may not be amiss.  It is well known to farmers that horse and sheep manure, under certain conditions, are very liable to ferment (compost, T. Visel) so rapidly as to get hot.  When this occurs, the manure grows white (part of the process of saltpeter formation known potassium nitrate, an alkali metal salt, T. Visel) and seems to have been burned.  The question is often asked me, Does this cause any loss to have such a thing happen?  I answer, Yes.  Almost the entire amount of nitrogen in a heap of manure may thus be driven out largely in the form of ammonia."

This bacterial transition in heat also occurred in marine composts as well as with bacteria that could withstand saltwater.  The farm community also knew that ammonia generation could occur in subtidal mud manures as well.  They once harvested coastal muds (harbor or mussel mud) as a soil nourishment called a top dressing.

Samples of harbor mud from rivers and bays as a soil nourishment or manure was often tested for fertilizer content – value.  Samples of harbor mud (called mostly mussel mud in northern New England) were sent in to the first Agriculture Experiment Stations for analysis and report.  A sample of harbor mud examined by the Maine Agriculture Experiment Station has this comment in 1885 – (my comments, T. Visel):

"This station was sent a sample (harbor mud, T. Visel) by Fred Atwood of Winterport (Maine, T. Visel) the barrel of mud was recovered weeks before being sampled and when it was opened, it emitted a strong odor of ammonia."

Certain bacteria can survive on the sulfate compounds in seawater.  The bacterial change would have a dramatic impact upon shallow water nitrogen levels.  As oxygen-requiring bacteria died out, the conversion of toxic ammonia to less toxic nitrate ceased or became minimal.  This allowed the level of ammonia to rise as its bacterial conversion to nitrate ceased (a long important function in aquaculture closed systems).  Ammonia surged into the water column and increased algal blooms, which then collected in the bacterial compost residues deposited on bay bottoms.  This impact, years ago, was sometimes described as a "marine snow."  This increased compost (often with strong sulfur smells) was also reported by coastal fishers as a deepening deposit of greasy, jelly-like substance that resembled a mayonnaise-like consistency.  Because iron is non-limiting and sulfides produce metal compounds, these organic deposits were a blue-black tint.  The term "black mayonnaise" can be found in many reports that describe this sulfide-rich deposit.  In time, these deposits can build to several feet deep.  (Even just a few tablespoons of this substance at room temperature can quickly fill a room with a strong sulfur smell.) 

Dredged channels and marina basins quickly could collect these deposits and, in high heat, become ammonia-rich, so much in fact that in 1994, the EPA had to modify its process for testing organisms for dredged material toxicity, urging laboratory technicians to rinse ammonia from dredged material samples so that toxicology tests could even begin.  This condition caused an emergency errata to be issued (it was suspected that ammonia was so high it killed the test organisms).

Following is an excerpt from EPA-600-R-94-0 25 June 1994: "Methods for Assessing the Toxicity of Sediment Associated Contaminants with Estuarine and Marine Amphipods" errata for pages 80-82:

"For dredged material testing, the following procedure should be used if it is necessary to reduce interstitial water ammonia levels.  Whenever chemical evidence of ammonia is present at toxicologically important levels of ammonia is not a contaminant of concern, the laboratory analyst should reduce ammonia in the sediment interstitial water to species – specific no effect concentrations.  Ammonia levels in the interstitial water can be reduced by sufficiently aerating the sample and replacing two volumes of water per day."

In other words, dredged material (especially high organic) could contain so much bacterial purged ammonia that it would kill test organisms.

That is why it is so important to look at these marine composts in low oxygen conditions as a potential huge nitrogen source (The proper name for these deposits is Sapropel – a composting bacterial process in the absence of elemental oxygen).  Sapropels can produce sulfides and impacts more than fish and shellfish species (bay scallops, for example, are acutely sensitive to sulfide) but also marine vegetation.  Sulfide is a plant toxin to seagrass, especially eelgrass, which like terrestrial grasses, gathers and holds organic matter.  For eelgrass in high heat, the sulfide build-up around its roots and kills the plant.  These events were recorded as "eelgrass death rings" – older plants which gathered organics died off first, leaving a ring of eelgrass, younger and with less time to gather organics alive.  Eelgrass that grew thick and gathered organic matter (in the historical fish and shellfish reports, a tendency for eelgrass meadows to rise from peat formation over time is often noted), which made it more susceptible to sulfide toxicity in heat or hot seawater.  Marine soils high in sulfides can cause the release of sulfuric acid when oxygen is reintroduced.

A bacterial change in heat, which shifted to sulfide formation of compost seawater chemistry, could kill or weaken eelgrass growths.  In addition, this compost chemistry could purge larger amounts of nitrogen dissolved in seawater and not eliminated as nitrogen gas.  In these conditions, bacterial denitrification would slow as the bacteria that converted nitrate to nitrogen gas freeing it from the water are gone, thus causing waters to become nitrogen-rich, mostly in the form of ammonia.  The bacteria that once converted ammonia to nitrate or nitrogen gas are absent because they cannot utilize sulfate as an oxygen source, leaving any plants or animals in these shallow waters vulnerable to intense sulfide poisoning – the rotten egg smell of late summer.  It is natural in warm seawater ammonia levels would now increase.

Sediment (soil) sulfide levels could possibly be one of the best indicators we have to detect massive changes in the bacterial – nitrogen pathways.  It is also a huge factor, in terms of marine soil health, for the growth of eelgrass and those plants in salt marshes.  Soils high in sulfide are toxic to eelgrass and Spartina patens (salt hay), which also does best in colder, more nitrate prevalent conditions. 

The recent eelgrass/nitrogen research controversy (2012, New Hampshire) centered on the growing conclusion that we targeted the wrong nitrogen source and chose the wrong environmental indicator to measure it.  One review highlighted the need to look at soil sulfides.  "Sediment sulfides were often not examined during these case studies as no applicable data were available."  (A connection to reducing nitrogen levels to increases in seafood assumed a steady state for oxygen availability.  In a warming climate, shallow waters hold less oxygen naturally and changing bacterial nitrogen from nitrate to ammonia is a natural result – T. Visel).  This above statement about sulfide case studies appears in a University of Connecticut eelgrass study that was referenced in a 2012 Nitrogen Review of the Nitrogen TMDL for Cape Cod (See Vaudrey, 2008 a/b, Establishing Restoration Objectives for Eelgrass in Long Island Sound).

Vaudrey – Review of the Seagrass Literature A-1, April 2008a, Sediment Characteristics

Pg. 24 –

"Eelgrass coverage was positively correlated with acid volatile sulfide in the sediments (Bradley and Stolt, 2006).  This is consistent with the observation that eelgrass beds will trap sediment and deposit leaves as detritus, increasing organic matter in the area, which in turn increases the chance of anoxia and hence the development of sulfide in the sediment."

Pg. 26 –

"Koch (2001) reviewed a number of studies to examine the effect of porewater sulfide concentration on eelgrass health and found indications that concentrations above 1mm may be toxic."

2008 Part B, Pg. 46, Vaudrey Case Studies 2008b, Sediment Characteristics

"The sediment quality is a necessary component determining the success of eelgrass in a particular site, but the tolerance of eelgrass for poor sediment quality seems to be greater if high levels are available.  Sediment sulfides were not examined during the case studies as no applicable data were available.  Very few studies here examined the critical thresholds for populations of eelgrass relative to sediment sulfide."

This University of Connecticut study was often a key reference as evidence that nitrogen reduction is beneficial and the reason (justification) to spend millions of dollars, citing eelgrass as an embayment health indicator (New Hampshire, 2012).  When looking at eelgrass today, its health is often guided by heat, bacteria and its natural ability to gather soil – composting organics.  Danish researchers in 2014 explained the loss (die-off) of eelgrass plants, sometimes referred to as "fairy rings" from sulfide.  Marianne Holmer from the University of Southern Denmark and Jens Borum from the University of Copenhagen linked these circular eelgrass die-offs directly to sulfide poisoning from mud collected amongst the eelgrass roots.  Older plants (more sulfide exposure) died in the center while healthy plants still lived in a ring of younger plants with less mud and, therefore, less sulfide exposure.  This die-off had a biology foundation as eelgrass traps organic matter (a natural characteristic of grasses); it becomes vulnerable if in high heat sulfide forms below the plant.  A bacterial switch to sulfate reducers (SRB) would doom shallow water eelgrass in high heat, especially if the eelgrass had collected over time a thick deposit of organic matter – a compost.  The surge in ammonia and formation of sulfide have a direct climate/bacterial link, both impacting the growth and survival of eelgrass, especially in shallow high thermal impacted waters.  Organic deposits in high sulfate waters can become a sulfide-rich sapropel in times of low dissolved oxygen.

Dozens of studies have indicated that most critical factor to eelgrass habitat quality is the amount of sulfides in the sediment (soil); some date back to the 1980's. Important sediment sulfide studies that could have pointed the nitrogen/eelgrass research in a very different direction were "forgotten" and perhaps misrepresented. This bacterial nitrogen appears to have a foundation in numerous TMDL documents – as exclusions of "second source" generation nitrogen in the formation of TMDL limits.  It is often called internal (fertilizer) nitrogen regeneration from sediments and therefore not "new" nitrogen or dissolved nitrogen attributed to human sources, such as septic systems.

Several nitrogen loading models (NLM) were developed under the assumption that the only nitrogen inputs were from watersheds (largely human inputs) or the atmosphere.  They often did not include the impact of organic bacterial composting processes nor the die-off of ammonia-oxidizing bacteria from lack of oxygen (or nitrate) in heat.  A large nitrogen source was often not included in many of these models – my view, T. Visel.

A major paper in Estuarine Coastal and Shelf Science 89 (2010), pg. 125-136 (2010) by James S. Latimer and Michael A. Charpentier titled "Nitrogen Inputs to Seventy-Four Southern New England Estuaries Application of a Watershed Nitrogen Load Model" describes excluding bacterial nitrogen on pg. 129 – (my comments, T. Visel):

"The NLM (Nitrogen Loading Model, T. Visel) is formulated to estimate nitrogen only from the local estuarine watershed to the small estuary; the only nitrogen loading source not from the watershed is atmospheric deposition directly onto the water surface.

Internal nitrogen regeneration from sediments and the water column is not considered in this paper; however, it is taken into account by the ELM.  The sediment has been ascribed by others to be a net sink (of nitrogen, T. Visel), except during summer periods where it may be a net source (Howes et al., 2003).  In either case, it is not "new" nitrogen, therefore, it was not included."

This could exclude natural bacterial actions that release nitrogen, especially in habitats prone to collect organic matter, such as embayments.  In the 1980's and 1990's, harbors and shallow embayments experienced a growing soft bottom organic deposit, often called a black mayonnaise by coastal residents.  This organic deposit in shallow inner harbors grew in depth and frequently suffocated shellfish beds.  It was first noticed by shellfishers and later those that fished for winter flounder over shellfish beds.  A 1987 Business Week article (October 12, 1987, pg. 98) by Russell Mitchell titled "An Oysterman's Battle to Keep "Black Mayonnaise at Bay" details these observations of Terry Backer, who would become the Long Island Sound Keeper in 1988 – (my comments, T. Visel):
"Toxic sludge – The three acre flat is the best thriving ecosystem in the otherwise dead inner harbor, according to biologists (often smells of sulfide, T. Visel).  Elsewhere, the bottom is covered by a thick layer of toxic sludge that fishermen call "Black Mayonnaise."  Were the mud flat destroyed, a spring flood or winter storm could flush the sludge into rich oyster beds that lie just downstream."

At this time, mono iron sulfide compost in heat began to form a sapropel.  As a result of bacterial composting in low oxygen, bacteria that changed ammonia to nitrate died off.  Ammonia levels now soared as organics (primarily leaves) collected to putrify in high heat.

The positive phase of the NAO (North Atlantic Oscillation) produced warmer winters and less storm activity.  When strong storms did happen, large amounts of sapropel (black mayonnaise) moved downstream as what occurred in Clinton Harbor following Hurricane Gloria in 1985.  Dams also hold back tremendous amounts of partially digested black organic pulp, and heavy rains wash this material to sulfate-reducing bacteria, which do not need oxygen and release sulfides as the composting process continues.  Dr. Vaccaro of Woods Hole Oceanographic Institution was testifying on this impact of organic enrichment from dumping dredge spoils before Congress (See Appendix #2).  But what are the consequences if Mother Nature dumped this organic matter, or from reducing tidal exchange or increase of heat this organic matter then – composted.  More recently, the impact of this deposit build-up over time, flowing over the Conowingo Dam, has come under research scrutiny (See EC #1: What About Sapropel and The Conowingo Dam?, posted September 29, 2014,  The Blue Crab ForumTM Environment and Conservation thread).  This compost can degrade habitat quality for years.  It is a huge source of nitrogen into shallow estuaries.

Consider the email I obtained from Dr. John Trefry of The Florida Institute of Technology in regards to the studies of black mayonnaise in the Indian River Lagoon Estuary.  On August 1, 2015, Dr. Trefry emailed me, responding to a question about bacterial generation of nitrogen.  He responded:

"We now have shown that at least half of the nitrogen introduced into the Lagoon is derived from fine grain, organic rich sediments on the lagoon floor.  It's all coming in as ammonium."

Second source generation of organic material (from leaves) is ammonia and with sulfate sulfide purging, is one of the most toxic of all substances to fish and shellfish.  High levels of ammonia with a whiff of sulfide will send any aquarium enthusiast into a panic.  This is a sign of bacterial filter collapse or failure.  This natural bay or cove "filter" is the bottom of shallow waters that consists of bacteria and organic matter.  When it is hot, the likelihood of ammonia purging increases and is measurable in closed seawater systems.

Blue Crab Biofilters First Used in 1969

Some of the first marine biological filters were designed for the soft shell blue crab industry to control toxic ammonia.  In the late 1970's, Steven Van Gorder developed bacteria – biological filters for closed systems (See Filtration Techniques for Small Scale Aquaculture in Closed Systems 1980 and Steven Van Gorder Fresh Culture Systems – Design of High Intensity Recirculating Aquaculture Systems – Proceedings Workshop held September 25 to 27, 1991, National Sea Grant College Program and The Louisiana Sea Grant College Program) with the goal of lessening toxic ammonia (See A Review of the Emerging Risks of Acute Ammonia Nitrogen Toxicity to Aquatic Decopod Crustaceans, Lin et al., 2022).

The concept was to duplicate the bacterial conversion of ammonia to less toxic nitrate and then to nitrogen gas.  This was a two-bacterial step – one strain converts deadly ammonia Nitrosomonas, releasing the nitrogen compound nitrite while the next converts nitrite to nitrate termed Nitrobacter.  Other bacteria converted plant tissue to ammonia with oxygen available during the entire process.  The first report of a closed system was developed by a Lake Ponchartrain blue crab fisher, Cultus Pearson, who operated a closed recirculating seawater system for shedders in 1980.  In Sea Grant Today, Linda Skupien of the Mississippi/Alabama Sea Grant Consortium details the Pearson Biological Filter developed by another blue crab fisher in the early 1970's.  From Skupien's 1983 article titled "Softshells Spark Enthusiasm" on page 6 is found the following segment:

"Within the filter, the layer of activated carbon screens out dissolved organic compounds, and the layers of dolomite provides the proper pH.  The layer of crushed shell houses two kinds of bacteria that keep the system clean.  "The biological filter evolved in the early 1970's with Lee Seymour, a Biloxi crab fisherman."

The biological filter duplicated the same bacterial nitrogen conversion that happened naturally.  This natural bacterial filter is today called "benthic flux" often without a nitrogen or bacteria connection.

The nitrogen pathway of nitrate (cold) and ammonia (heat) is often described as a benthic flux, a confusing term if it lacks a nitrogen cycle explanation (my view, T. Visel).  But this is the bacteria in nature – consisting of different species of bacteria that can fix nitrogen from air, as well as convert nitrate to a gas and convert ammonia to nitrate.  Forgetting or omitting bacterial nitrogen sources (benthic flux) gives imprecise nitrogen data if not identified.

A USGS study contains the following segments:

(Quantifying Benthic Nitrogen Fluxes in Puget Sound, Washington – A Review of Available Data.  Scientific Investigations Report 2014-5033, US Department of The Interior US Geological Survey by Richard W. Shiebley and Anthony J. Paulson) contains the following:

Page 3:

"The amount and quality of organic matter delivery to the sediment surface determines the amount and form of N (nitrogen) mineralized from the sediment as well as the sediment oxygen demand (SOD)."

Page 2:

"In Puget Sound, Washington, ignoring or underrepresenting benthic flux as a source of N to marine waters can result in ineffective management actions and can lead to chronic water quality problems in sensitive areas.  Shallow areas near the shores of Puget Sound are most likely to experience low levels of dissolved oxygen because of the combination of low relative circulation, warm summer water temperatures, and proximity to watershed nutrient contributions, sediment nitrogen fluxes may also dominate in these shallow areas."

{This compost is also termed Benthic Flux, Sapropel, Black Mayonnaise, Gyttja-See The Norwalk Hour 10/21/2012, Saugatuck River, Dick Harris, Southern Life University Newsletter, August 2011 Vol.14 #6 Sound School Southern New Haven Harbor Collaborative, pg. 1., Dr. Vince Breslin}.

Also implicated in this growing eelgrass/nitrogen controversy is the association of eelgrass and other submerged aquatic vegetation commonly called "SAV" to specific estuarine health indicators.  SAV became an environmental lightening rod so to speak to galvanize public opinion and then public policy makers as to protect and conserve SAV habitat types in the 1980's and 1990's.

In New England, eelgrass was first promoted to benefit the bay scallop, a much-admired delicacy in our bays and coves. While lightly populated SAV patches are beneficial as reef habitats in long periods of heat and little storm activity, dense SAV meadows collect organic matter, which then sheds ammonia in heat and purges toxic sulfides in winter.  Massachusetts state shellfish reports contain references to thick eelgrass growths as harming shellfish populations, even the bay scallop in the 1960's and 1970's.

In the end, dense SAV (Ulva lactuca) becomes nature's sulfide-killing fields, signaling the end of periodic habitat succession. It is deadly to shellfish and finfish larval stages and in dense mats sheds ammonia a key nutrient ingredient for brown algae also called Harmful Algal Blooms or "HAB" for short. A huge source of ammonia is second source generation from organic deposits and was not, I suspect, included in many nitrogen TMDL reports. 

The shellfishers on Cape Cod correctly called the SAV/shellfish relationship decades ago, but no one believed them. How could the shellfishers be correct when nearly all of the current scientific community was promoting the eelgrass/bay scallop model? In this situation, quite simply, the Cape Cod shellfishers "nailed it."  In the end, thick eelgrass became more of a foe than a friend to shellfish – even at times, to the bay scallop.

They already had seen what large SAV monocultures could do to shellfish.  This shellfish suffocation was included in several State of Massachusetts reports up until 1972.

Dense thick growths of submerged aquatic vegetation suffocate living shellfish and destroy habitat capacity for future shellfish populations.  It will take a change of energy often with temperature to restart this cycle or habitat succession.  In areas of little current, this organic paste can accumulate quickly and often black from iron compounds with a strong sulfide smell.  A recent Cape Cod Report for Wellfleet, Massachusetts found that "black custard" had organic levels as high as 21% (See Center for Coastal Studies "Black Mayonnaise" in Wellfleet Harbor: What Is It and Where Does It Come From?, May, 2020, 25 pgs.).

The law of habitat succession or those of us who have fished and shell-fished in New England's coves and bays and have seen eelgrass come and go in long term natural cycles share a different view. The habitat history of eelgrass is very different than what have been portrayed to the public even to the shellfishing community itself. We know from historical records (mostly from the State of Massachusetts) that dense eelgrass meadows were not beneficial for all shellfish populations and in fact now it seems that bay scallops will set in eelgrass not as a preferred settlement type, but perhaps to escape bottom predation from the eelgrass meadows below. Early bay scallop studies clearly documented "blade attack" from crabs and that redweed, Agardhiella subulata, also served as a settlement type for bay scallops.  The source of these reports was the bay scallop fishers from Niantic Bay, Connecticut. These reports and historical documents report that dense eelgrass monocultures destroyed numerous New England shellfish habitats but were not referenced in eelgrass studies of the past four decades.  In Europe, the green crab (an invasive species here) has a direct habitat relationship to eelgrass meadows.  John Hammond on Cape Cod felt that "our" eelgrass was carried here aboard the first ships from Europe.  He detailed that the Cape Cod strain thrived after strong storms and cooler waters.  This was a cultivated "new sand" signal to eelgrass habitat improvement.  Over time, however, it was doomed in shallow water when it was hot.  These areas released the smell of rotting eggs – sulfide aerosols.
Eelgrass Nitrogen TMDL Review

It appears EPA strongly promoted the nitrogen linkage to eelgrass health to perhaps bolster regulatory authority under the Clean Water Act, EPA Region 1 (See Meetings & Minutes of EPA Eelgrass Research Team) also strongly promoted the nitrogen TMDL without fully considering the sediment respiration of bacterial nitrogen (Benthic Flux) and now complicates some aspects of nitrogen models (my view, T. Visel). This is especially true in terms of the law of habitat succession (See Daniel Pauley, Shifting Baselines, 1995) or marine habitat succession over time (Rhoads, 1985).  Changing temperatures could alone greatly influence nitrogen generation in shallow embayments.  Those are the areas that often have the warmest waters and greatest areas of organic composting – much of it from terrestrial organic sources.

Eelgrass Health Indicators Are Climate Related

Eelgrass, like other terrestrial grasses, has a "habitat clock" or in times of history subject to change "value" according to the law of habitat succession in the marine environment. That is, any habitat services must be indexed with habitat change as plant species mature and exchange dominance on land.  Habitat succession in the marine environment does not stand still; therefore, snapshots that portray a lasting goal or benefit or contain constant habitat values are misleading at best and biased for habitat succession. It is certainly something upon which not to base long-term public policy objectives.

The scientific community last February (2014) was startled by reports from Denmark that eelgrass was dying off from sediment sulfide toxicity. For some of us following the eelgrass research since the 1980's we were not surprised. Some of the historical research conducted a century ago (also in Massachusetts) by David Belding clearly detailed observance of eelgrass holding organic matter in high heat.  The source of sulfur emissions and negative sulfide changes or direct impacts to shellfish species, all of them including bay scallop. In the end, the sulfur compounds (sulfide) became so high it killed off eelgrass directly or weakened it so as to experience increases of fungal/slime mold infections. At the end of hot seawater temperatures bacteria are linked to creating vast mud flats unable to sustain any shellfish sets.  Many researchers in the late 1990s identified the sulfide formation as a habitat constraint and toxic impacts to eelgrass itself. Some of this pioneer sulfide toxic submerged aquatic vegetation research was conducted in Tampa Bay, Florida.

A Long Term Environmental History is Important to Coastal States

Beginning in 1871, and under the auspices of the Smithsonian Institution, we saw the first U.S. records of fish and shellfish landings that could be indexed for climate/energy factors and important eelgrass observation5 made over 150 years but not reported in the scientific literature – in fact, much of this climate bias could have been prevented by a good balanced long-term environmental fisheries history. Nitrogen TMDL criteria formulated by ignoring organic primary and secondary (bacterial) source compost nitrogen compounds are incomplete and now the subject of recalibration efforts, especially as predicted waters will continue to warm.

An environmental history is very much needed as a bias in the research literature is being discovered in salt marsh studies (1971-1981) and also dredge windows (1985 to present).  Eelgrass in cool energy-rich waters provide important habitat "services" to many species, but those waters are enriched with organics, which have quite opposite habitat values in heat and need to be included and fully addressed - my view, T. Visel.

The connection to abundant eelgrass and the bay scallop has a direct water temperature connection to energy.  Bay scallops are acutely sensitive to sulfide, and sulfate bacterial metabolism in organic deposits is deadly.  When in shallow water, they are both most damaged or killed by high sulfide-containing waters.

GAO-14-80 Dec 2013 Report to Congressional Requesters

"The water resource experts reported that about half of the TMDLs they reviewed do not contain key features helping to ensure that implementations can be done, which leads to TMDLs that may do little to actually improve water quality," pg. 4, GAO-14-80 EPAs TMDL program.

"TMDLs without certain key features may be unlikely to help water bodies attain water quality standards and may potentially waste states limited resources ibid" – pg. 64.

Research Funding and Programs Need to Include Climate Change

In light of the lack of historical information and bias with carefully scripted RFP nitrogen research proposals, omissions of both historic/period research and actions of public policy makers reflecting upon such research a funding relief action could be required. Peer review from the scientific community itself is not sufficient against science/research bias as evidenced by long-time habitat history eelgrass case6.

(Congress investigated EPA review panels and reaffirmed the National Academy of Science, National Research Council and the Science Advisory Board protocols, which serve EPA, were re-coded in 2001 for conflict of interests. Findings showed transparency improved but did not exclude as qualified review members, who often worked or benefitted from some of the same policies or obtained grant funds for research areas that they were asked to review. See the report for the 2012 Cape Cod TMDL review panel.)

Nitrate Reduction Removed A Key Sulfate Buffer – Toxic Sulfides – Have We Possibly Targeted the Wrong Nitrogen Compound for Removal?

As more information is available from overseas (mostly Denmark), the removal of nitrate in high heat facilitated the production of second source ammonia, in other words, it made low oxygen impacts only worse. In the marine environment during high heat, sulfur and oxygen sediment reducers turn to nitrate when oxygen compounds are lowered (this is called limiting). Removing nitrate will allow sulfur-reducing bacteria to quickly access seawater sulfate (electron affinity), which is not limiting in the marine environment. Therefore nitrate reduction is now linked to increases in deadly sulfide/sediment formation. Nitrate buffering sediments with high leaf (organic matter) content purge sulfides in winter and shed ammonia compounds in summer, ammonia is now linked to the toxic brown algal blooms termed Harmful Algae Blooms (HABs).

A requirement may be needed that all estuarine research be subject to an impartial "Environmental History Impact Statement" to bring balance to NEPA policies – my view, Tim Visel.

The description of all negative environment impacts must somehow be attributed to just human action has resulted in some extreme conservation protection policies. Although public policy intervention in the 1950s and 1960s had very firm foundations (Love Canal, New York and Cuyahoga River Fire, Ohio), this has created a "baseline dilemma" as historical reviews were eclipsed by human existence "insulting nature," which was used quite effectively with the eelgrass/nitrogen indicators.  Sometimes nature itself causes what we view as negative impacts or pollution – naturally.

Much of the basis of the NEPA Act was to ascertain any (all) human impacts to the environment, usually in response to coastal development within federal funded projects. The requirement of Environmental Impact Statement or "EIS" itself needs to be balanced by a mandatory review of natural long-term climate and energy cycles for the coast. Much of the controversy and confusion surrounding the 1999-2004 lobster die-off for example a review of historical records would have shown that it resembled (almost precisely) the die-off of lobsters here before 1898-1905. In both cases, blue crab abundance suddenly soared after each lobster die-off as what recently happened here again7.  This previous lobster die-off, however, was rarely mentioned after the more recent lobster die-off.

7 Note: The DEEP Marine Fisheries office has 130 years of historical records of fish and shellfish reports, lobster hatchery records (hatcheries were built in New England following the 1898 lobster die-off) as well as hundreds of fish census files and boxes of other historical fin and shellfish reports.

Records of Native American shell middens may represent one of the few unbiased measures we have in determining the natural cycles of fin and shellfish species abundance, free of human climate/energy change discussions. The need of a long-term, unbiased environmental history is therefore critical.  One of the concerns of grants spent "about" issues rather on how to mitigate them.  Taxpayers are often left with large, thick reports but little tangible, environmental or economic results.  Some projects (funded with general tax obligations – US citizen taxpayers) contain little long-term resource or economic benefit other than increased public "awareness."   

Nitrogen, Eelgrass & Climate

In light of the dramatic change in climate patterns recently and the dramatic habitat reversal in which we appear to be in, the heat and low energy conditions could return.  The last transition period lasted from 1922 to 1972 with 1931 to 1971 being a period of strong coastal storms and colder winters.  In 1993, EPA itself recognized the role of microorganisms in the nitrogen cycle.  EPA 625/R-931010, September 1993, A Process Design Manual for Nitrogen Control, pg. 20, 1993, includes the following:

"Ammonification, nitrification, synthesis and denitrification can occur within the aquatic environment.  Ammonification of organic matter is carried out by microorganisms.  The ammonia thus formed, along with nitrate, can be assimilated by algae and aquatic plants for synthesis.  If excessive, such growths may create water quality problems."

The recent weather pattern change, since August 2011, has resembled the end of The Great Heat 1880-1920, a four-decade period that witnessed decreasing energy and increasing temperatures.  Climate patterns should be reviewed in oxygen levels as they respond positively with colder temperatures and naturally contain less oxygen in heat.  The oxygen inverse solubility law is one of the most prevalent biological laws; it certainly deserved some attention in the TMDL discussions (my view – Tim Visel).  In periods of heat, many reports exist in the historical literature of massive microalgal blooms, such as "sea cabbage" today called sea lettuce (Ulva) (See New England Lobsters Make a Comeback in 1912, posted July 31, 2019, The Blue Crab ForumTM).

The changes in sediment characteristics and the use of sapropels in many estuaries along the eastern seaboard (i.e., Indian River EPA Estuary Program, Florida) should raise a review of organic nitrogen inputs.  These can be natural, such as reforestation or human waste of nitrogen with the use of fertilizers.  It is becoming apparent that a large organic nitrogen source (organic matter) was missed in previous TMDL discussions.  This appears to have created a biased TMDL process that placed more emphasis on human source nitrogen while ignoring organic inputs that, in high heat, has far greater ecological change than aqueous nitrogen compounds.  In my opinion, we need a full impartial review.  While programs to remove human nitrogen can be done, their impacts relating to cyclic climate patterns may have little influence upon seafood abundance.  Other factors such as tidal restrictions or flushing rates may have much larger nitrogen roles.  This is noticeable in coves with tidal restrictions.  It is the shallow waters that the oxidation of organic matter is most noticeable as mentioned by Selman A. Waksman and Margaret Hotchkiss in an article in the Journal of Marine Research No.1, Vol. 2, pgs. 101-118, 1937-1938 "On the Oxidation of Organic Matter in Marine Sediments by Bacteria":

"Of further significance is the fact that the rate of oxidation or organic matter from bottom deposits nearer to land and from shallower basins is considerably greater than that from bottoms at greater depths and distances.  The organic matter in these bottoms is much more resistant, the oxidizability being only one-tenth or one-fifth of that of the organic matter in shallower bottoms near land." (pg. 116)

Of great significance is not all bacteria access oxygen in the same way.  Significant bacterial processes rely on other compounds that contain oxygen, such as nitrite, nitrate and sulfate, to name a few.  For example, anammox bacteria convert ammonia to nitrogen gas but needs nitrate NO2 as an oxygen source to complete the process.  When nitrate and nitrite are limiting, other bacteria fill voids that can utilize sulfate as an oxygen source.  Sulfate is nonlimiting in marine waters.  Therefore, bacterial sulfate metabolism (sulfide) has a direct link to eelgrass habitat quality, especially in heat and low elemental oxygen conditions. 

We need to review all natural bacteria nitrogen processes and how they interact with habitat values under different seawater temperatures – my view, Tim Visel.

Appendix #1

King's Mark Resource Conservation & Development Area
Environmental Review Team
Sackett Hill Road
Warren, Connecticut 06754


Sulfur enters Frash Pond in the form of sulfate dissolved in seawater.  Saltwater being denser than freshwater remains at the bottom of the pond even when the surface water is fresh.  During the summer, solar heating at the surface further intensifies the density differences between the warm fresh water on top and the cold saltwater at the bottom.  The strong density gradient drastically reduces mixing in the pond, causing the saltwater at the bottom to become stagnant.  Isolated from the atmosphere, the bottom water rapidly gives up its dissolved oxygen to the respiration of organic matter in the pond sediments. 
Respiration consists of two linked processes.  First, organic matter gives up electrons as it is oxidized to carbon dioxide.  Second, an electron acceptor receives those electrons and becomes reduced.  In aerobic respiration, the electron acceptor is oxygen, which is reduced to water.  However, when ambient oxygen is exhausted, bacteria have the ability to continue oxidizing organic matter by using alternate electron acceptors.  Sulfur is an excellent alternate electron acceptor for anaerobic respiration by bacteria.  Initially sulfate can be reduced to elemental sulfur, and then elemental sulfur can be further reduced to sulfide.  Both sulfur products bear upon the situation at Frash Pond.
First, elemental sulfur is very insoluble, and quickly precipitates out of water.  This raises the possibility that the sediments of Frash Pond have been enriched in sulfur during various periods of its history.  Second, sulfides are very insoluble in the presence of metals, precipitating as black metallic sulfides, which give marine muds their inky, blue-black appearance.  Thus, the bottom of Frash Pond also may have been enriched in metals.  These include potentially toxic heavy metals introduced from nearby landfills.  Third, when sulfide is more abundant than the constituents with which it is insoluble, sulfide appears as soluble and volatile hydrogen sulfide.  The evolution of hydrogen sulfide gas which calls attention to Frash Pond each summer is but the tip of the sulfur-cycle "iceberg" which operates in the depths of the pond all year.
To summarize, there are four basic components to the problem with sulfur at Frash Pond:

1.   Source of sulfur: Sulfate in seawater and, possibly, sulfur enriched sediments.
2.    Stratification: Chemical and thermal density gradients in the water column.
3.   Organic matter: The electron donor driving the reduction of sulfate to sulfide.
4.   Potential metal toxicity: Possible pollution from nearby landfills.

Appendix #2

Available Nitrogen and Phosphorus and the Biochemical Cycle in the Atlantic Off New England1
Ralph F. Vaccaro
Woods Hole Oceanographic Institution
Journal of Marine Research, Pg. 284-301
Journal of Marine Research, Sears Foundation for Marine Research, Yale University
PO Box 208118, New Haven, CT 06520-8118 USA

'Contribution No. 1357 from the Woods Hole Oceanographic Institution. This research was supported by the U. S. Atomic Energy Commission under contract AT (30-1)-1918 and the National Science Foundation grants NSF 10709, 8544, 8339, and 544·


The importance of ammonia as a source of available nitrogen for phytoplanktonic populations off New England has been evaluated for August and January 1962. During August, when only trace amounts of nitrate persist in the photic layer, ammonia appears to be the major source of available nitrogen. Therefore, meaningful estimates of the relative amounts of nitrogen and phosphorus being assimilated at such times require consideration of the nitrogen occurring as ammonia. Total available nitrogen: phosphorus ratios of change have been derived from the sum of the nitrogen occurring as ammonia, nitrite, and nitrate and from the concentration of phosphate. These ratios have been compared with other data (for August and April) based on the organic nitrogen and phosphorus content of particulate fractions separated from suspension by Millipore filtration and by net tows. The results indicate that the ratios of change for August are somewhat lower than those for January and that the former are accompanied by a comparable depression in the N:P ratios for particulate material separated by Millipore filtration. It is speculated that during late summer, when nitrate and nitrite concentrations are minimal, ammonia forestalls the extreme degree of nitrogen deficiency known for laboratory cultures of nitrogen-starved algal cells.

Introduction. The amount of ammonia-nitrogen within the euphotic layer of the sea is often an important part of the total nitrogen available for protein synthesis by marine phytoplankton. However, estimates of the nitrogen reserve for the reproduction and growth of these organisms have often included only measurements of the nitrogen present as nitrite and nitrate. A previous study of the nitrogen and phosphorus cycles in New England coastal waters (Ketchum et al., 1958) was also based on insufficient ammonia data, although amino-nitrogen was cited as a possible additional source of this element. At the same time, the need for simultaneous observations on the organic nitrogen and phosphorus content of coastal planktonic communities, especially during periods of nitrate depletion, was stressed.
Previous measurements for these waters have revealed how surface N:P atomic ratios, based solely on nitrogen as nitrite plus nitrate, approached zero as summer progressed due to a quantitative removal by September of nitrite and nitrate. On this basis the native phytoplankton would necessarily appear to assimilate these elements at a higher ratio than that presented to them in their native habitat. However, ammonia-nitrogen is also a suitable source of nitrogen for these organisms and must also be seasonally evaluated, especially, for the summer months, before a realistic opinion of the degree of plant adaptation to the summer quantities of available nitrogen and phosphorus is possible.
The depletion of nitrate during late summer from the waters of Long Island Sound has been described by Riley and Conover (1956).  Ketchum et al. (1958) have shown that low, summer nitrate concentrations comparable to those of Long Island Sound are widespread and extend seaward to the more oceanic surface waters off the New England coast.

Results. The maximum ammonia concentration in the shallower waters south of the Cape occurs close to the bottom, suggesting the accumulation of important nitrogen contributions from ammonification within the sediments. As shown in Figs. 2a and 2b, the August nitrogen:phosphorus ratios for the layers of active plant growth approximate zero both northeast and south of the Cape unless ammonia is taken into account.
In January, following the breakdown of the summer thermocline, the waters south of Cape Cod are quite homogeneous with respect to inorganic plant nutrients (Fig. 2c). High concentrations of nitrate (ca. 8.0 µg A/l) and phosphate (0.8 µg A/l) are the rule throughout the entire water column, while ammonia concentrations, though irregular, remain comparable to those observed in summer. These winter nitrate concentrations are sufficiently high to relegate ammonia to a minor fraction of the total available nitrogen, and the influence of ammonia then is at a seasonal minimum.

Discussion. By late summer, nitrogen assimilation by marine phytoplankton in the surface waters off New England has reduced nitrate to trace amounts close to the limit of sensitivity of the analytical method employed. Overall, the winter-to-summer decrease in nitrate exceeds twentyfold. Ammonia persists, however, throughout the summer at about half of its winter concentration, and by August it has become the more abundant source of plant nitrogen.  Conversely during winter, although higher concentrations of each type of nitrogen are present, nitrate-nitrogen is five or six times more abundant than ammonia.  Unlike nitrate, phosphate appears to be present in excess amounts throughout the year.
It appears that the relative abundance of ammonia as opposed to nitrate during summer in the euphotic waters off New England coincides with maximum stratification of the water column due to increased surface temperatures. High nitrate concentrations, which persist throughout the year at subeuphotic depths, become progressively more isolated from the surface as the seasonal decline in solar radiation approaches.  With high stability, nitrate enrichment of the surface waters is ultimately minimized because of reduced vertical mixing across a strong thermocline.  Until the occurrence of active nitrification within the upper layer is more conclusively demonstrated, it must be assumed that, at such times, the major impetus to the nitrogen cycle is provided by ammonia because of its more rapid exchange between organisms and environment and because of its direct addition from the atmosphere in association with rain (Menzel and Spaeth, 1962).

Appendix #3

Assessment of the Effects of Bottom Water Temperature & Chemical Conditions, Sediment Temperature, Sedimentary Organic Matter (Type & Amount) on Release of Sulfide and Ammonia from Sediments in Long Island Sound: A Laboratory Study 2004
EPA Long Island Sound Project Descriptions
Final Report Summary


Dr. Carmela Cuomo, University of New Haven
Dr. Paul Bartholomew, University of New Haven

Final Report Summary

The goal of this research was to investigate how certain factors in the environment of Western Long Island Sound interact to cause a release of ammonia and/or sulfides, at certain times of the year, from the sediments of WLIS. Factors investigated included: water & sediment temperature, initial water dissolved oxygen (DO) levels, additional of organic matter (plankton), sediment organic content, and the presence or absence of organisms in the sediments. The main findings of the project are as follows: 1. addition of fresh plankton is a significant influence on the release of both ammonia and sulfides from bottom sediments in WLIS. Addition of fresh plankton results in an increase in the release of ammonia from sediments while it results in a general decrease in sulfide release from bottom sediments. 2. The influence of bioturbating organisms on sulfide and ammonia release from WLIS sediments, while not significant (! < 0.10), is present and varies with the other conditions present (i.e., DO, temperature, plankton). 3. The influence of water column DO content on ammonia and sulfide release from sediments is significant but it varies with other factors. 4. The influence of sediment locality on ammonia and sulfide release from sediments, while present, was not significant by itself. However, when taken with plankton, DO, and temperature, locality does exert a significant effect – especially upon sulfide release. Locality was selected as a proxy for organic carbon content. 5. The strongest and most consistent influence on ammonia and sulfide release from sediments under experimental conditions was temperature – both water column and sediment temperature. Sediment temperature consistently tracked water column temperature and ran, on average, 2oC higher than water column temperature. The results of this work demonstrate that temperature, dissolved oxygen, and the addition of plankton, such as happens during the Spring and Fall plankton blooms, all play a significant role in the release of sulfides and ammonia from WLIS sediments. Furthermore, the study suggests that sediment organic content further influences such release.

Appendix #4

Summary Report

Technical Review of Select Memorandums Supporting the Development of Nitrogen Endpoints for Three Long Island Sound Watershed Groupings: 23 Embayments, 3 Large Riverine Systems, and Western Long Island Sound Open Water

January 29, 2019

Prepared for: U. S. Environmental Protection Agency Region 1
U.S. EPA Contract Number 68HE0118A0001
Order Number 68HE0118F0006

Prepared by:
HydroAnalysis, Inc.

On behalf of:
PARS Environmental, Inc. & Comprehensive Environmental, Inc.

3. Is it ecologically valid to assume that total nitrogen (TN) is conservative (i.e., that it is not being removed from the system in significant amounts) for the purposes of this modeling effort?
Dr. Bierman's Response

Nitrogen was not part of the hydrodynamic modeling effort described in Subtask E. The memorandum states that results from this effort for dilution of salinity will be used as a proxy for nitrogen dilution under the assumption that nitrogen within embayments is approximately conservative. This assumption is not generally valid, especially within embayments and nearshore areas. Not only will there be some settling and volatilization losses, as the memorandum states on Page E-1, but there will also be gains due to sediment diagenesis and the resulting sediment-water diffusion of nitrogen. These processes are complex and can vary in both space and time, especially between embayments and open water areas.

As an example, in their linked watershed-embayment modeling study of the Pleasant Bay System, Massachusetts, Howes et al. (2006) investigated sediment-water exchanges of nitrogen. Howes et al. (2006) Figure IV-20 (below) is a conceptual diagram showing seasonal variation in sediment nitrogen flux. During summer (i.e., the primary period of interest identified in Subtask E), sediment-water nitrogen flux is at maximum values. Howes et al. (2006) Table VI-2 (below) contains total nitrogen loads for individual sub-embayments. The loads for net benthic flux were based on site-specific measurements during the summer period. For most of the individual sub-embayments, and for the system as a whole, net benthic flux of nitrogen to the water column was larger than external nitrogen loads from the watershed itself. For the Pleasant Bay System, the assumption that nitrogen within sub-embayments is approximately conservative is violated by greater than a factor of two.

Appendix #5

Volume 16, Issue 1, July 1976, Pages 1-7
Formation of mackinawite by the microbial reduction of jarosite and its application to tidal sediments
K. C. Ivarson, R. O. Hallberg

A study was made of the microbial reduction of jarosite (K Fe3(SO4)2(OH)6), a mineral formed by the aerobic iron-oxidizing bacterium Thiobacillus ferrooxidans, and frequently found in acid sulfate soils developed on marine sediments containing pyrite (FeS2).

Under anaerobic conditions and in the presence of organic matter (lactate) and the sulfate-reducing bacterium Desulfovibrio desulfuricans, jarosite was soon reduced to a sulfide — a poorly crystalline form of mackinawite (FeS). Due to the presence of phosphate ions in the cultural medium, vivianite or its polymorph metavivianite (Fe3(PO4)2.8H2O) was formed also. Because aging transforms mackinawite into pyrite, it is suggested that in marshy areas where pyritic sediments and acid sulfate soils ('cat clays') occur, and where aerobic and anaerobic conditions exist, there is a generic relationship between pyrite and jarosite and the above two microbes help to maintain this relationship by cycling sulfur and iron between the two minerals. At the same time they perhaps aid in cycling phosphorus.