EC #26 - Bacterial Ammonia from Sapropel Deposits

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EC #26 - Bacterial Ammonia from Sapropel Deposits
Eelgrass/Sapropel Linked to Ammonia Generation in Heat

View all Bacteria/Nitrogen Posts on The Blue Crab Forum™ on the Environmental Conservation Thread
The Danger of a Warming Planet

The Benthic Generation of Ammonia in Warm Waters
Revised 2021
When It Came to Fish and Shellfish, Did We Look At the Wrong Nitrogen? – Revised 2012
Nitrate Buffering and the Role of Sulfate Metabolism in Nitrogen Levels of Shallow Waters
This is a Delayed Report
Tim Visel retired from The Sound School June 30, 2022 Viewpoint of Tim Visel, no other agency or organization


Preface

This report has been revised from 2012 to November 2019 and updated to 2021.  It was in outline form presented to the CAC of the Long Island Sound Study to express concerns about nitrogen loading of Long Island Sound and the role of bacterial responses to organics (leaves, grass clippings, bark, etc.) flowing into our coastal areas.  In "closed" aquaculture systems, the use of bacterial culture medium had been used for decades to reduce toxic ammonia to less toxic nitrogen compounds such as nitrate.  I was fortunate to work with Steven Van Gorder in the late 1980's with rotating contact bacterial biofilters to reduce ammonia in some of the first tilapia closed recirculating systems.

Since that time, more and more information regarding natural bacterial filter systems for nitrogen has been published. In fact in areas close to the coast or waterways homeowners are being urged to modify septic systems for bacterial bio-reactors.  These bacterial reactors (often highlighted as a new process) use the action of a low oxygen bacterial process that takes nitrate as an energy source and by doing so releases nitrogen as a gas (N2).  This is called Anaerobic Digester and can produce biogas or methane.  The gas, however, also often contains H2S hydrogen sulfide.  This is an ancient process and one that is well known in aquaculture – the bacterial biological filter.  The biological aspect here being the natural action of bacteria converting ammonia to nitrate and nitrate to the gas (N2).  This bacterial action tends to remove nitrate and by doing so reduce natural and unnatural nitrate levels.  This is done in the presence of oxygen, however, an Anaerobic Digester (AD) is not oxygen-dependent.  When ammonia oxidizing bacteria die – ammonia levels increase, with a shortage of nitrate requiring bacteria nitrate levels increase, the latter action more in cold while ammonia levels tend to rise in heat.  This is a well known aspect of coastal waters and reviewed in 1963 by Ralph F. Vaccaro of the Woods Hole Oceanographic Institution in a report funded by the National Science Foundation (contribution No 1357 from the Woods Hole Oceanographic Institution) on page 290-291 has the comment, - Journal of Marine Research, "Available Nitrogen and Phosphorus and the Biochemical Cycle in the Atlantic Off New England," which relates to temperature, my comments (T. Visel):

"In spite of this stability difference, ammonia-nitrogen is consistently more abundant than nitrite and nitrate – nitrogen within the upper 30 meters in August both Northeast and south of Cape Cod.  At the Gulf of Maine stations, where the water column extends to much greater depths than just south of Cape Cod, nitrate exceeds ammonia – nitrogen below 30m and relatively large concentrations of the former apparently persist throughout the year.  The maximum ammonia concentration in the shallower waters south of Cape occurs close to the bottom, suggesting the accumulation of important nitrogen contributions from ammonification within the sediments.  In January, following the breakdown of the summer thermocline, the waters south of Cape Cod are quite homogenous with respect to inorganic plant nutrients.  High concentrations of nitrate and phosphate are the rule throughout the entire water column (this research was completed in the height of a negative NAO – winter and fall storms thoroughly "mix" bottom and surface waters – T. Visel) while ammonia concentrations, through irregular, remain comparable to those observed in summer.  These winter nitrates concentrations are sufficiently high to regulate ammonia to a minor fraction of the total available nitrogen, and the influence of ammonia then is at a seasonal minimum."   

Bacteria Organic Matter and Heat

Inshore waters also have this seasonal reverse and ammonia levels soar in hot summers.  This is from the change of bacteria consuming organic matter and what oxygen source they utilize to obtain the energy to do it.  This reversal in nitrogen is more evident in shallow waters where waters are susceptible to wide swings in temperature.  In the Indian River Lagoon (Florida), The Florida Institute of Technology is monitoring this surge in ammonia.  Following is a quote from an email I obtained from John Trefry on August 1, 2015:

"Hi Tim –

We have now 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.

Best regards,
John"

A clearer habitat picture is evolving for fisheries habitat quality as it relates to natural nitrogen inputs.  A long-term view is critical to more fully understand the impact of nitrogen upon finfish and shellfish populations.  This paper is a revision of a 2012 nitrogen research caution about the focus upon linking nitrogen to living marine resource abundance and the need to fully evaluate all estuarine water nitrogen sources for Total Maximum Daily loads (TMDL) estimates.  Since 2012, the climate here (New England) has turned cooler with much more energy and heavy rains that washed huge amounts of organic matter into estuaries.  Since then, we can anticipate a dominant long cycle of sulfate bacterial nitrogen introduction to occur in heat.  Much of that nitrogen may enter water ways as a result of a bacterial sulfate reduction process, bacteria that digest or break down organic matter in the form of dead plant tissue with the use of sea water sulfate as an oxygen source.  All that requires is a return to warmer summer temperatures and mild winters.  This would allow blooms of algal species that survive on high amounts of ammonium – these are often referred to as the "browns."

At the same time, sulfate reduction by sulfur-reducing bacteria can now produce profound habitat change.  Sulfate reduction of organic matter, (sealed from oxygen) unconsolidated leaf organic detritus, consolidated salt marsh, peat, and bog deposits all alter nitrogen inputs. Increased access to sulfate from a rise in sea level raises additional concerns about sulfuric acid and toxic heavy metals, especially aluminum discharges from salt marshes.  In high heat, such marshes can also become toxic to many shellfish and finfish larval forms from sulfides (these are referenced by bad, low tide smells in August).  Continued warming will have dramatic impacts to fish and shellfish habitats we consider important in shallow water habitats.  Areas that collect organic matter and naturally set in motion bacterial composting processes are the ones to monitor for high ammonia use of phytoplankton.

The amount of nitrate builds up in coastal waters when it is cold.  Bacterial release occurs when oxygen levels are highest.  This is the nitrogen that feeds the phytoplankton spring blooms that are the food for shellfish.  As spring blooms happened, nitrate became limiting as ammonia levels increased.  This was studied in 1950's (Long Island Sound), a time period now known as a negative NAO.  A key report was issued in June 1959 – Oceanography of Long Island Sound, Vol. 17 – Bulletin of The Bingham Oceanographic Collection, Yale University (153 pages).  G.A. Riley in Oceanography of Long Island Sound 1954-1955, pg. 18, reviews the nitrate in Long Island Sound, which contains this segment:
"From the end of the winter flowering until August or September, there was little or no nitrate anywhere in the water column except for a small but noticeable increase in April of each year in the eastern most area."

And further –

"Early in the survey, the poverty of nitrate suggested that nitrogen might be a limiting factor with respect to phytoplankton growth."

Eugene Harris details the Nitrogen Cycle in Long Island Sound reviews this nitrate limitation.  Page 32 Bulletin of the Bingham Oceanographic Collection – The Nitrogen Cycle:

"The winter maximum of inorganic nitrogen, mainly in the form of nitrate, was almost entirely removed from the water column during the late winter diatom flowering."

The relationship of bacterial release of nitrogen was known as a significant source of nitrogen for plankton.  Harris mentions this bacterial release on page 59, which has this segment:

"The role of bacteria has not been examined directly, but it may be deduced from the foregoing discussion that they supplied some 20 to 40% of the daily phytoplankton requirement."


Did We Look At The Wrong Nitrogen?

One of the most important issues facing nitrogen reduction programs is realistic assessment of nitrogen enrichment.  If nitrogen TMDL levels were directly linked to dissolved oxygen concentrations, they were most likely set to levels that were not calibrated to warming waters.  Compared to some 1971 water quality (Long Island Sound) documents, warming waters alone would have naturally reduced oxygen levels needed to prevent anoxic conditions that favor sulfate bacteria.  Several comments made at a July 2015 EPA workshop at the University of Connecticut (Avery Point) admitted the LIS nitrogen model was not calibrated for climate change.  Proceedings of the Long Island Sound Water Quality Workshop, July 14 and 15, 2015, UCONN Avery Point Campus, Future Developments in Monitoring Technology Moderators UCONN Jim O'Donnell and Mike Twardowski, Florida Atlantic University, Breakout Session raw notes, pg. 17 – I posed this question:

Tim Visel – We need to consider benthic flux of nitrogen (biochemical process) Jim [O'Donnell UCONN] said that "we need to monitor benthic areas too in order to understand this process further." 

The connection to nitrogen reduction to increases in seafood abundance needs to be reviewed in terms of climate change.  Warmer waters naturally contain less oxygen and natural (bacterial) organic respiration would have, itself, create anoxic conditions (dead zones).  The accepted Biological Oxygen Demand (BOD) of organic matter is 30mg of O2 are utilized by bacteria to reduce organic matter over 5 days per liter of water.  A high organic loading would cause an oxygen demand that may bring oxygen content to zero.  Hot water naturally contains less dissolved oxygen and river waters often carry heavy organic loads after heavy rains.  The mouths of rivers that naturally carry organics to the sea in hot weather will likely experience an increase of "dead zones." 

It is also natural that hurricanes would wash huge amounts of organic matter into shallow waters – food for bacteria.  This organic matter flush has a negative residual impact often called the "green manure effect."  This organic matter can suffocate bay bottoms – turning them black and sulfide rich.  This happened when excess organic matter is added.  It can be human (organic matter), such as suspended solids from sewage treatment or nature.  This is also termed the "green manure" or green leaf effect.  A strong coastal storm may wash millions of tons of windblown leaf paste into coastal bays and coves.  Here, in slow moving waters, it settles and becomes a bacterial source of ammonia or sulfide, a sulfate metabolism bacterial component of "black water" in rivers with high tree pulp or sawdust.  The state of Maine experienced this sulfide generation in rivers with sawdust and wood pulp.  This green manure aspect was carefully detailed in 2008 following Hurricane Gustav in Louisiana.

Chesapeake Bay inshore fishers now experience the same organic suffocation and nitrogen enrichments process below the Conowingo Dam which holds leaves, stems, blossoms and other plant residues as compost that flows out an over shallow water habitats after severe storms (See EC #1: What About Sapropel and the Conowingo Dam, posted September 29, 2014 on The Blue Crab ForumTM Environmental Conservation thread).   

These two case histories provide examples of sulfide formation by bacteria, one that happened in Louisiana and one in Maine.

Green Leaves and Hurricane Gustav Hits Louisiana – Atchafalaya Basin Keeper®

This case history involves a day-by-day timeline from when Hurricane Gustav hit Louisiana's coast September 1, 2008 as a strong category 2 storm, almost a category 3. This is a valuable report as it occurred in a relatively low population area and gives a detailed report on the impacts of leaves entering low energy waters (from the Hurricane Gustav Fish Kill Report and Case History – Atchafalaya Basin Keeper®

On Monday, September 1st, huge amounts of green leaves into area waterways and forests, commonly known as the Atchafalaya Basin. Wednesday, September 4th – flooding occurs as heavy rains now enter waterways.  On Thursday, September 5th, the water in wooded areas starts to smell "like raw sewage" and the writer refers to it as "the green manure effect."

September 6th finds dead and dying fish – waters are flooding with millions of gallons of green leaves, now going into the basin watershed.

The report continues, "the effect of green leaves in water is very different from dry, brown autumn leaves rotting the water. Fish are coming to the surface."

September 7th reports dropping water levels but massive fish kills of shad, catfish, carp, buffalo white drum, perch (several species) and bass (all species). The only fishes that lived were garfish, bowfin and minnows.

September 8th – Pat's Bay suffers 100% kill of all fish; horrible smell starts

September 10th – Black water comes out of Sorrel Shellfield Bayou. Black water mixes with muddy water of Bayou Sorrel. Egrets observed feeding on sick fish. Black water looks black and thick and smells like raw sewage.  Fish are taking refuge in Mound's Bayou.

September 13th – Hurricane Gustav makes landfall in Texas. Very strong winds push bad water back into basin worsening water quality that now has a horrible smell.

September 17th to 18th – Water quality improves.  Fish again observed in some areas. Although in some areas it continues to be very bad – Shellfield.
Conclusion: "Our observations suggest that massive fish kills following hurricanes are caused by green leaves falling into the water and decaying" (Report of the Atchafalaya Basin Keeper®)

Paper Pulp and Maine's Androscoggin River

Other case histories involve the paper industry, which uses a process that utilizes sulfate reducing bacteria to break down pulp wood chips (very similar to marine breakdown of leaves in the marine environment) to produce a thick, black water fluid called black liquor. Before paper industries regulated waste products (which they do today), they often discharged black water into rivers and streams. In one of the most detailed case histories (which are now available on the internet) titled "Defining a Nuisance: Pollution, Science, and Environmental Politics on Maine's Androscoggin River."  In 2012, Wallace Scot McFarland in a paper on environmental history (Environmental History, 2012, 17(2), pages 307-335) details the social, regulation and economic issues confronting residents along the Androscoggin River, which at the time had several pulp and paper mills. It is some of the observations in the article (and this one in particular) highlights the Tannin (brown water) sapropel black water cycles.  Following is the opening quote from the McFarland article:

"In 1941, along Maine's fetid Androscoggin River, houses freshly painted white turned black as hydrogen sulfide rising from the water reacted with paint, a direct result of polluting from upstream pulp and paper mills. Inside Leo Good's drugstore, the river odor was so strong that "people would order ice cream and go away without eating it."

The Androscoggin River is an important case history for the Saprobien (organic wellness index) system developed in Europe in the 1900's.  The Saprobien system looked at the negative impact of organic matter (human and natural) as an oxygen-depleting activity of bacteria, especially in European rivers (See Kolkwitz and Marsson, 1902).  Similar impacts were recorded in US rivers that obtained huge quantities of organic matter, mostly forestry products.  We have the records of Edmund Muskie, US Senate (1959 to 1980) and Dr. Walter Lawrence, a Bates College chemistry professor (See Marine History online – Clean Water: Muskie and the Environment), who was named Androscoggin River Master in 1948.  From Maine History online is this segment about organic pollution of the Androscoggin River:

"Since the 1880's when paper mills began creating pulp with a sulfite chemical process, water downstream of paper mills often smelled awful."

And further –
"A study of the Androscoggin in the early 1940's showed that it had almost no dissolved oxygen."

Senator Muskie and the citizens of Maine experienced the "organic wellness" of the Androscoggin of horrible smells and dead fish. [Senator Muskie helped draft and introduce the Clean Water Act on October 28, 1971 to the US Senate for a floor vote.  It passed 86 votes yea and 0 votes nea.  A year later on October 18, 1972, his bill became law.]

Dr. Lawrence, in his efforts to maintain some oxygen in the Androscoggin, introduced sodium nitrate as a secondary oxygen source.  His use of nitrate was similar to the introduction of nitrate into Point Judith Pond, Rhode Island fifty years before by Dr. George W. Field.  Dr. Field had also noticed a shortage of nitrate during warm summer fish die-offs in the 1890's.  His efforts were to introduce it to help feed algae that needed nitrate to live, important forage for shellfish.  After elemental oxygen is fully utilized, bacteria that can utilize nitrate can still survive to break down organic matter.  The use of nitrate for a source of oxygen is today termed nitrate buffering (bacterial denitrifying) for bacteria that use nitrate instead of oxygen, thus sparing any elemental oxygen in the water.  As hot water (fresh or salt) naturally contains less dissolved oxygen, bad sulfur smells or fish kills occur most often in heat. 

In warm cycles, species appear to reverse here; in colder times, species change again.  A bias now is apparent as many nitrogen model/reduction projects may highlight warm periods but don't address cold cycles/periods.  Temperature and energy levels have significant impacts upon fish and shellfish.  While nitrogen plays an important role, it is estuarine benthic habitat quality that plays a dominant role, nature's nitrogen filter systems.  This bacterial filter system often found in recirculating aquaculture production modules have a two-step nitrification process that converts ammonium (deadly to fish) to a less toxic nitrogen-nitrate.  Step 1 has nitrosomonas changing ammonia to nitrite and then as step 2 nitrobacters changing nitrite to nitrate (an excellent presentation of this process is online – See John R. Buchanan, PhD, Department of Biosystems Engineering and Soil Science, University of Tennessee Agricultural Experiment Station, Waste Water Basics 101).  A third step is the release of nitrogen as a gas or N2 (this is the concept of denitrifying wood chip septic bio-reactors).  This process detailed in the agriculture studies of soil bacteria a century ago is today being described as "experimental septic bio reactors" on Cape Cod.

Bacteria & Nitrogen

A need exists to review information on bacterial population shifts and the impacts upon nitrogen recycling.  New research is highlighting the role of natural filter bacteria called Anammox strains, which can remove ammonia in low oxygen conditions.  Research now indicates that in addition to buffering sulfate digestion, it also could sustain bacterial strains that naturally strip ammonia from coastal waters.  To remove ammonia from seawater, an extremely toxic compound to sea life, anammox bacteria, under anaerobic conditions can utilize nitrite to convert ammonium to nitrogen gas (Brin et al., 2014 Limnology Oceanographer, 59 (3), 2014, pgs. 851-860).  Re-oxidation by forced physical mixing by hurricanes is now suspected to restore oxygen bacterial strains in shallow water benthic organic deposits.  Colder water naturally contains more oxygen and buffers the change to higher ammonia.  Higher ammonia levels have been linked to the "brown tides" harmful algal blooms (HABs) of the 1980's.  This is a period of warming coastal waters.  The relationship between ammonia and nitrate from bacteria is missing from many TMDL studies (Total Maximum Daily Loads) of a pollutant. 

The lack of a long-term assessment that would have covered climate cycles in the TMDL (my view) is one that did not include dramatic dissolved oxygen shifts from temperature and energy patterns acknowledged in testimony about the TMDL process. Page 37 of a 2000 public comment expressed a similar concern about a point in time nitrogen measure guidelines for Long Island Sound:

"Moreover, if a decision were rendered that the 1988 hydrodynamic conditions were too "extreme" and that protecting water quality for 1989 conditions (once in 5-10 year event) was sufficient to protect fishery resources, the entire complexion of the TMDL would be changed, even for New York waters" (CT Water Pollution Abatement Association CWPAA Testimony Submission, January 28, 2000 – Response to Public Comments on The Long Island Sound Draft Total Maximum Daily Load Analysis To Achieve Water Quality Standards for Dissolved Oxygen Long Island Sound, December 2000, CT DEP).

In time, we may learn that in periods of heat and low energy, natural bacteria filter systems develop slowly to accommodate nitrogen imbalances.  This, in turn, changes the timing and species constituents of resulting algal blooms, such as the browns (HABs) that devastated New York bay scallop populations.  Several bacterial species were noted to thrive on ammonia while many species preferred the colder bacterial component of nitrate.

As the EPA Long Island Sound study formed, some of the issues regarding fishery habitat histories discussed at Coastal Cove and Embayment meetings and blended into some EPA discussions in the mid-1980's as living marine resources.  I expressed concern then as seafood did not necessarily follow nitrogen levels, nor were long habitat changes often included in the TMDL, and now climate change, it seems (July, Avery Point workshop comments to questions, 2015). 

Recently, more information is coming to light that not only was nitrogen removal improperly linked to seafood abundance, but by removing human nitrogen as possible oxygen source constituents (nitrite and nitrate), we have perhaps compromised nature's long-term natural filter systems for removing ammonia from seawater naturally low in oxygen (Source: "The Environmental Controls That Govern the End Product of Bacterial Nitrate Respiration," Kraft et al., Science 8, August 2014, Vol. 345, pg. 676-679).  This lack of oxygen might be the equivalent of nature pulling the plug on aquarium filter systems; when the filter stopped, ammonia levels soared.  Was it the filter or "nature" pulling the plug on it the cause of higher ammonia? 

I was suspicious of the nitrogen removal link to a natural filter failure or a respiratory failure or sulfide toxicity just as those utilized in aquaculture systems when temperatures are raised see (EC #8: Natural Nitrogen Bacteria Filter Systems, posted October 30, 2015, The Blue Crab ForumTM) and when almost every advanced wastewater treatment plant on the east coast utilizes bacteria in filter systems.  The role of nitrogen as secondary oxygen sources is linked to that of bacteria, and as such, often not included in TMDL.  In fact, from recent reports, it was both the hard nitrogen (plant tissue) was not measured for TMDL and the fact that with sulfate, an oxygen containing compound that is not limiting, is the key oxygen ingredient for sulfur-reducing bacteria ammonia purging, both can be missed by analytical measurement data.  The nitrogen models created from such compromised data, will, without doubt, fail or be so inconclusive as to be of little value to current habitat and/or seafood discussions – my view.

Two Different Nitrogen Cycles

The short nitrogen cycle (nitrite nitrate) typically is a cold-water nutrient important for spring algal blooms.  The long nitrogen cycle is dominated by the warm water presence of ammonia that supports late summer HABs (Harmful Algal Blooms), which need high ammonia levels.  That is why the green algae is a cooler "spring bloom" (nitrate requiring) while the browns are usually in late summer and fall "blooms," which thrive in ammonia.  Long Island Sound in the late 1980s had several brown tide outbreaks; shoreline waters from air surveys clearly showed a band of brown along Connecticut's coast.  The dominance of browns soon was apparent to even casual beach goers in hot summers.  The long nitrogen cycle (ammonia), one that has a bacterial component, is formed by organics.  Organic matter on the bottoms of coves and bays rots, similar to terrestrial composts, only in the marine environment low oxygen levels open a bacterial sulfate reduction pathway.  This happens during periods of heat and low level energy is when ammonia levels soar.  This pathway utilizes sulfur-reducing bacteria with very damaging impacts to oxygen-requiring organisms; they can continue to consume organics without elemental oxygen.  The presence of sapropel (a marine compost) also acts to smother oxygen bacterial filter systems and sheds toxic compounds especially sulfides.  As much attention was directed to the short nitrogen (human sources), very little attention was given to benthic flux, a term that loosely describes this bacteria sulfate nitrogen factor, which in most cases was noticeable by fishers in the 1980's (Cape Cod Times article titled "Scientists Seek Input on Oxygen Depletion" dated Thursday, July 5, 1984, See Appendix #3).  The water, at times, seemed to smell "bad" or contained "sulfurous muds."

We Need To Review Nitrogen Removal Programs

Although many TMDL documents include atmospheric source nitrogen and organic matter deposition (manure), they fail to disclose the full nitrogen cycle and the consequences of organic matter in hot shallow waters, "the nursery areas for fish and shellfish," or include at all the impacts of sulfate reduction.  I learned at an EPA water quality workshop in July 2015 (under direct questioning) that our Long Island TMDL-nitrogen Sound model was not "calibrated" for the increase in the forest canopy here in Connecticut now estimated at 78% nor the increase in seawater temperatures in the 1990's (climate change).  When organic matter was included into the TMDL process, it was attributed to improper forestry practices or increased erosion (both linked to negative human activities) in many TMDL estimates/models on the Atlantic coast.  Today, Connecticut has more trees and paved surfaces increasing the flow of organics (mostly ground leaf and grass) into estuaries (See Appendix #1: USGS Urban Leaf Litter Study). 

The return of trees to New England would also bring more leaves.  This was quite noticeable in the alewife runs on Cape Cod in the early 1980's.  According to Joe DiCarlo (known as "Buzzie" to his colleagues at the Division of Marine Fisheries in Sandwich) who supervised the maintenance and installation of herring runs in Massachusetts (See Anadromous Fish Investigations, Massachusetts AFC-1, February 1, 1967 to June 30, 1970, PL 89-304, Anadromous Fish Act), small streams filled with leaves in the 1970's.  This is described in the above report as "It is recommended that the section of stream below the first dam be brushed out and cleaned of debris to improve access."  However, the impact of leaves would block streams and slow flows so that remaining alewife suffered predation.  The influence of organic matter and low dissolved oxygen and high ammonia (toxic to alewife) and noticed in waste water as high ammonia-nitrogen content downstream of sewage outfalls.  Page 15 of the 1970 report found that in the Taunton River minimum dissolved oxygen of .3mg/L and maximum ammonia-nitrogen of 1.22mg/L were recorded in July 1970. (Ammonia has a high oxygen demand and increases the oxygen requirement of fish.).  By 1981 when I worked on Cape Cod, low flows (the Cape was in a severe drought) and in increase in leaves filled many alewife runs.  This happened as leaf burning bans were enacted in New England (New York Times, November 22, 1981, Leaf Burning Ritual Evolves Many Constraints Across U.S.).  Few composting programs existed, so leaves were often dumped in waterways instead of the custom of street-side burning, which released nitrogen into the smoke.  Now leaves on paved surfaces were ground into a brown organic pulp and washed into streams and then estuaries.  I can recall each fall in the 1960's people would rake leaves into the side of streets, ignite them and reduce them to ash/carbon residues.  Rainfall would then remove these ashes into watersheds.  Increased organics in hot dry periods would enhance nitrogen bacterial release in the estuaries – evidence by foul marsh odors – the smell of sulfides.

In small coves and bays, the sulfate reduction of organic matter and ammonia generation from sulfur-reducing bacteria was at times "missed" and possibly attributed to human inputs under a mass balance formula that did not discriminate between ammonia sources – the ones now attributed to sulfur-reducing bacteria utilization of the sugars locked in straw, manure, hay and leaves.  Ammonia is the byproduct of sulfate reduction and those coves that had high sulfate levels changed by marine waters started the first brown algae blooms – increase of shallow waters and heat killing off the "good bacteria" in tidally restricted areas occurred here first and first noticed by eastern Long Island baymen by the changes in clear bottoms once trawled and scalloped by dredges.  These once had bottom habitats over time had turned soft and soupy. (Inshore fisheries, especially bay scallops, quickly declined after the buildup of foul muds).

Areas once clear or clear consisting of sands and pebbles now had eelgrass leaves and became "foul" and often bad smelling in the 1980's (See Appendix #2: Studies Urge Action On Waterford's Coves).  Others commented that the bay scallop grounds now had, in time, this organic matter putrified and started to generate ammonia, which now because of tidal restrictions (both man-made and natural) ammonia levels increased, and in the heat, brown algae blooms bloomed again as they did in the 1900's.  In these bays, ammonia now sloshed back and forth with the tides, feeding dense blooms of brown algae.  Eastern Connecticut baymen may recall that the brown algae blooms occurred in the upper reaches, the ones poorly flushed first and spread out slowly into deeper bay waters.  These hot water brown tides were devastating to eastern Long Island bay scallops.  It also signaled an increase in bacterial sulfides.  Bay scallops are extremely sensitive to sulfide.  The FAO reports that bay scallop A. irradians stops feeding at .7ppm (See Appendix #5). 

Ammonia from sulfate digestion of organics has long been an issue from a once prosperous New York duck farm industry.  Sulfate reduction was also studied a century ago when, in times of little concern, sawdust and waste wood chips were dumped into New England's rivers.  The reduction of wood waste resulted in the first "black water deaths" and similar organic pollution gave rise to the European Saprobien System Index of Species based upon energy, temperature and organic matter pollution overseas.  The term sapropel, the putrefaction (reduction) of organic matter in the absence of oxygen, is widely used in Europe.  This index is termed the "organic wellness system" and noted how long moving water could cleanse itself of excess organics with sufficient oxygen.  I was first exposed to bacteria using nitrate as an oxygen source on Cape Cod.  Here, the Hyannis wastewater treatment plant had increased aeration of digestion pools to keep oxygen levels high to keep the biological bacteria filters "alive."  The aeration had sent the strong odor of ammonia to neighboring homes and calls to the Cape Cod Extension Service and my visits to the area.  In a meeting with Plant officials a few days later, during the meeting it was suddenly announced that "Nitrate levels were dropping" and caused concern with plant operations staff.  It was explained to me that when nitrate levels dropped, the oxygen bacterial filter process was near collapse.  In effect, the use of nitrate was a "last chance for those oxygen bacteria to survive."  The nitrate was an oxygen source buffer to the prevention of "black water," the collapse of the filters.  (The same black sulfide line could be seen in early aquaculture bio filters – T. Visel)

The concept of nitrate buffering the impacts of sulfate reduction is frequently not mentioned at all (except perhaps waste water systems still using biological filter systems) in the TMDL documents I have read.  Here bacterial strains would have a war as those that needed oxygen (elemental) and nitrate (compound) oxygen to survive, and the removal of nitrate (termed nitrate buffering) is now being linked to sulfate reduction.  If your TMDL documents do not include bacterial sulfate reduction, your nitrogen model and TMDL documents may contain a data bias – my view.

In the numerous TMDL documents and reports I have read, they strive to link human source, residential and agriculture nitrogen, to fish and shellfish habitat degradation.  Without full disclosure and review of long-term organic inputs, fall leaves in northern regions and wasted green manure in the southern areas, these documents give readers an imperfect conclusion habitat wise for finfish and shellfish.  In fact, the removal of a nitrite and nitrate also removed a form of oxygen compounds at the same time.  The largest problem overall with many nitrogen TMDL documents is the use of the term "sediment" and failure to include it as a marine soil once it is in an estuary.  Sediment gives readers a public policy and recognized concept just of erosion from land.  While this alone is a problem, most of the "sediment" damage that occurs in shallow warm habitats is not from direct burial (winter storm sand deposited in the 1960's and 1970's is a large New England problem as it impacted herring and alewife runs), but from biochemical bacterial organic matter decomposition (composting) known to impact these marine soils since the 1930's.  Failure to disclose these bay bottoms of having bacterial soil characteristics adds to the scientific bias and now it appears, perhaps, possible research misconduct if an organized attempt is to deflect a full nitrogen discussion or review. (Note: Organic matter in seawater is referred to as suspended solids as milligrams per liter).  In some New England dredged basins organic composting can fill them in a short time with an organic ooze frequently termed a "black mayonnaise." It was known in 1994 that such dredge deposits had very high ammonia levels (See EPA Errata (1994a) for dredge material testing of estuarine/marine amphipods).

In 1994, EPA recognized that dredged material had ammonia levels so high it exceeded toxic levels for pollution test organisms.  Page 39 of "Evaluation of Dredged Material Proposed for Disposal in New England Waters," New England District, April 2002, US EPA, US Army Corps of Engineers has this segment:

"Because amphipods and mysid shrimp are sensitive to sediment ammonia, renewals of overlying water are allowed to reduce exposure.  Excessive ammonia concentrations may cause mortalities in these species and confound the mortality end point of interest to the dredging regulatory program." 

And further –

"Ammonia toxicity changes as ephemeral environmental conditions, such as temperature, salinity, oxidation state and pH change.  To account for this potential false positive, the EPA and Corps (Army Corps of Engineers, T. Visel) have devised methods to reduce ammonia toxicity before and test begins" (Sections 11.4.5 to 11.4.5.3 of the EPA Amphipod Manual (EPA 1994a) as amended by the "Errata" sheet for pages 80 to 82 of that document).

The eelgrass monoculture was also connected to nitrogen pollution and promoted as a key or most important habitat type.  This is not conjecture.  Only a glimpse of the volumes of eelgrass literature will show its promotion with or without nitrogen policies while other habitat types, kelp-cobblestone or bivalve estuarine shell, had nowhere near the grant emphasis compared to that of eelgrass.  Eelgrass, perhaps, fulfilled many policy (regulatory) objectives, such as bottom disturbance (as evidenced by numerous eelgrass bottom disturbance policies), nitrogen reduction, and environmental protection (mapping, conservation and eelgrass preservation policies).  The latter is evidenced by existing regulatory policies after 2006, efforts aimed at New England legislatures and subsequent eelgrass protection legislation at the state and federal levels.  Habitat types or maps making the connection of eelgrass abundance to nitrogen abatement policies are frequent.  Estuarine shell (oysters) as a habitat type helps reduce acidic conditions from sulfuric and tannic acid (global warming), helps other fish and crab species (reef services), contributes to shellfish production (a food), and helps filter seawater, improving UV light penetration, yet is not even recognized as a distinct habitat type.  (This was recently changed in 2018 – T. Visel).

Not only are many of the environmental policies attached to eelgrass/nitrogen policies may be deeply flawed but they also oppose global warming chemistry.  The fact of the matter is eelgrass helps global warming habitat destruction in the very shallows; it lives by speeding habitat succession and a rise of sulfides.  This aspect of habitat quality and succession can be traced back to the beginning of oyster aquaculture, those so called natural shellfish beds, ones that exhibited over time (not snapshot) better habitat quality for certain types of species of shellfish in different climate conditions.  These areas did not naturally obtain an oyster set.  This was changed by the input of energy – clearing silt, flipping oyster shells or placing new shell "cultch."  To obtain oyster sets and oyster growth habitat constraints were removed by "work" or succession energy.

Many New England states, including Connecticut, have strived to distinguish "natural beds" or perhaps more suitable soils of habitats defining those areas not available for aquaculture or designation.  Several issues emerge – the concept of work to improve habitat conditions to enhance marine soil chemistry (similar to agriculture), the placing of oyster shell prior to oyster setting, for example, with the ability to change soil characteristics (such as pH by adding shell) and in those areas not formerly productive (pest control) or the placement of predator protection nets.

Duplicating in a way the natural cycle of soil succession – cultivation, increasing pore water circulation and even changing the bacterial benthic species includes eelgrass soil composition (pH).  Similar to nitrogen, the emphasis on eelgrass as a habitat indicator is subject to climate change. It was long thought that such soil cultivation was beneficial to the growth and survival of clam species. It is.  Much of the bottom disturbance policies have a foundation of conservation, that preventing bottom disturbance will increase shellfish production.  Many of these areas are termed preserves but do not "preserve" populations from storms, heat or cold, or organics from land.  The Connecticut oyster industry did maintain spawning beds in creeks but every five years they were dredged, organics removed reshelled and planted with adult oysters as "spawners."  (In other words, they applied work so that habitat succession could commence – again).  The accumulation of organic matter over once large oyster beds was documented in Maine around the turn of the century (Castner, 1950).

In the 1960's and 1970's, large areas of once certified grounds were closed to direct shellfish harvesting.  (An excellent review of this aspect can be found in "Best Management Practices for Shellfish Restoration" by Dorothy Leonard and Sandra MacFarlane prepared for the ISSC Shellfish Restoration Committee, 2011.).  This situation could be considered the largest shellfish "sanctuary preserve" effort in the United States.  Unfortunately deprived of culture or harvest energy, many shellfish habitats succeeded to those that often held few shellfish species of value but at the same time tended to contain benthic species that could tolerate higher sulfide levels (and predatory clam worms).  This habitat change is often recorded by inshore fishers as a transition from firm or soft bottoms to those that became soft and sulfide-rich.  In 1990, Sandra MacFarlane of Orleans, MA conducted a study, which included a survey noting bottom firmness.  Most surveyed noticed a trend of previous harder, firm bottoms were now becoming soft 44%; only 4% of the survey returns reported soft bottoms becoming firm (See 1999 – revised in 2004 – Bay Scallops in Massachusetts Waters-A Review of the Fishery and Prospects for Future Enhancement and Aquaculture, Barnstable County Cooperative Extension and Southeastern Aquaculture Center). 

The concept of setting off preserves as a conservation effort will not, over the long-term, provide what was intended.  Canada's experience with marine preserves found that habitat succession was evident (sulfide suspected) and did not preserve species targeted "species of value" (See Benthic Studies of Bideford Reserve, pg. 7, Fisheries Research Board of Canada Manuscript of the Biological Station St. Andrews, No. 1014, January 1964 to December 31, 1964):  Contains this statement,

"Clean shell on muddy bottom caught no shell bed fauna.  This may be an indication that gross change from clean to muddy bottom is an irreversible process."

In published research, Rhoads and Germano (1982) found that successional organisms transitioned to sulfide-tolerant organisms that reworked sapropel known as tube builders – Arthropoda species.  These organisms can tolerate high levels of sulfide and were often termed "tubiculous amphipods" for their ability to build tubes in sulfur rich sapropels.  (Interpreting Long Term Changes In Benthic Community Structure: A New Protocol.  Donald C. Rhoads and Joseph D. Germano.  Hydrobiologia 142: 291-308 1986 keywords, benthic monitoring, animal sediments, remote sensing (See Appendix #4).
   
Conservation missions combined with a pollution, regulatory authority became a powerful agenda for nitrogen removal.  In time, we may need to review if the ends justified the means – was removing nitrogen a bad concept?  No, not necessarily.  Everyone has seen what happens to the farm pond next to the manure pile in August.  The foundation of nitrogen removal did have a foundation in truth but the promises of seafood abundance did largely ignore climate and energy impacts.  Climate patterns (NAO) could lead to cycles in habitat quality for fish and shellfish abundance as well.

Perhaps the largest issue with nitrogen removal is that is also removed oxygen bound to it.  That is rarely mentioned as both an aspect of sulfur reducing bacteria (SRB) or that SRB will never be limited by a lack of elemental oxygen.  They use sulfate and a readily abundant seawater source of oxygen bound to a sulfur atom.  Sulfate reduction and glucose metabolism have been studied since the 1930's.  It is sulfate reduction that produces the ammonia and sulfide, the high heat/low oxygen reduction of organic matter without elemental oxygen. 

In heat, we may see little nitrogen reduction other than a change of nitrogen compounds.  We can learn much by reviewing the relationship between nitrate to ammonia in shallow water and that will require a close look at climate change – my view, Tim Visel.

APPENDIX #1

Chesapeake Bay News, November 21, 2016

USGS Urban Leaf Litter Study - Posted in Environmental Issues

The Chesapeake Bay, like most American estuaries, suffers from excess nutrient runoff.  A recent U.S. Geological Survey (USGS) study suggests that urban leaf litter removal might be one tool to help reduce phosphorous and nitrogen in nearby waterways. 

According to USGS, Autumn leaf litter contributed a significant amount of phosphorous to urban stormwater, which then runs off into waterways and lakes.  Excessive amounts of nutrients like phosphorous and nitrogen can cause eutrophication, or the depletion of oxygen in water, resulting in death of aquatic animals like fish.

The USGS-led study found that the timely removal of leaf litter can reduce harmful phosphorous concentrates in stormwater by over 80 percent in Madison, Wisconsin.

The study found that without removal, leaf litter, and other organic debris in the fall contributed 56 percent of the annual total phosphorous load in urban stormwater compared to only 16 percent when streets were cleared of leaves prior to a rain event.

"Our study found that leaf removal is one of the few treatment options available to environmental managers for reducing the amount of dissolved nutrients in stormwater," said Bill Selbig, a USGS scientist and the author of the report. "These findings are applicable to any city that is required to reduce phosphorous loads from urban areas."   

The study also found that stormwater nutrient levels were highest during the fall months when the amount of organic debris on streets was at its peak.

This finding suggests that leaf removal programs are most effective during fall in Madison, and that sources other than leaves, such as street dirt and grass clippings, were likely the primary contributors of phosphorous and other nutrients during spring and summer.


APPENDIX #2

New London Day – December 3, 1983



"WATERFORD - After three years of study, the answer is clear.  If something is not done about Waterford's coves, the town will lose the valuable resources.

This is the message the Flood and Erosion Control Board will bring to the Board of Selectmen Tuesday.  The board will attend the 7:30 p.m. session at Town hall to present the results of studies conducted to determine the effects of siltation on the delicately balanced resources and to ask the selectmen to request state money to take action against the problem.

"The town has an obligation to maintain its coastal resources.  The problems experienced are due to various acts by man... therefore, man should intervene in some of these cases to reverse a process he certainly has played a key role in," said John A. Scillieri Jr., chairman of the Flood and Erosion Control Board.

Among the man-made creations affecting the coves are railroad bridges, roads, filled in portions to support building and dams.

Scillieri's presentation Tuesday will include slides of Alewife, Keeney, Smith and Jordan coves to help illustrate problems existing there and outline possible methods for stopping future deterioration and reversing existing damage.

Dredging the coves would improve water circulation which would in turn upgrade the quality of the coves, Scillieri said.  Other actions would be taken to eliminate sewerage that still runs into some coves and caused nutrient imbalances that lead to foul cove odors in warm weather.
 
"The town is losing valuable resources.  It is losing navigational boating interests, the water quality is suffering and recreational interests are continuing to suffer," Scillieri said.  "Some recreational opportunities will disappear if nothing is done."

The local board is not alone in its concern for the coves, or in its ability to document the danger they are in. Several studies by groups contracted by the board and the Planning and Zoning Commission also conclude that action must be taken to save Waterford's coves.

"I think the problem that we've seen in the coves will continue and in some cases, they will continue to worsen," Scillieri said.  Among the specific concerns are that Alewife Cove's deterioration could at some point adversely affect Ocean or Waterford beaches, to which it connects. Also, in this and other coves, shell fishing, regular fishing, boating and other recreational activities could be hampered or obliterated if the deterioration is allowed to continue, Scillieri said.

A municipal coastal study, authorized by the planning commission to help it comply with state coastal management directives, recommends that water quality can be improved in several ways.  Among them are limiting constrictions on tidal circulation, limiting sedimentation resulting from changes in the areas around the coves and fostering cooperation with East Lyme and New London, which share two local coves.

It also recommends that shell fishing be encouraged and expanded, along with recreational opportunities for Waterford's coastal resources.


Appendix #3

SCIENTISTS SEEK INPUT ON OXYGEN DEPLETION

(Article sent to Tim Visel by John Hammond)

PAGE 8 CAPE COD TIMES, THURSDAY, JULY 5, 1984



Upton, NY – Marine scientists at Brookhaven National Laboratory are conducting a research study dealing with oxygen depletion of salt water along the mid-Atlantic coast, from North Carolina to Maine.

They would like to receive first-hand reports from shore residents and others who are familiar enough with a body of salt water to recognize some of the unusual or abnormal things that occur as a result of oxygen depletion. The study deals with salt water only in coastal areas or in estuaries, not with fresh water.

The scientists are interested in information on the following things, particularly if they have occurred since 1970: fish kills, red tides, algae blooms or scums, unusual smells (especially sulfurous bottom mud), the disappearance of "regular" marine life (fish, plants, or birds), and the appearance of "new" marine life.

The results of the research study will be important to people who live in coastal areas because oxygen depletion can destroy marine resources, particularly fish and shellfish.

Anyone who can contribute information is invited to write or call Terry Whitledge, Ocean Sciences Division, Brookhaven National Laboratory, Upton, NY 11073; telephone xxx-xxxx.


Appendix #4

Long Term Changes In The Benthic Community

From Rhoads and Germano Hydrobiologia pg. 291-308, Vol. 142, 1986 "Interpreting Long-Term Changes In Benthic Community Structure: A New Protocol" pg 301 contains this section, my comments, T. Visel (   )

(Key words – benthic monitoring, animal-sediment, remote sensing)
A major research issue in benthic ecology that needs to be addressed is the determination of the critical organic loading rate for stage III seres (series) i.e., the rate which causes their local extinction.)

Once this is known, the datum (a fixed starting point) may prove valuable for managing anthropogenic (human pollution, T. Visel) inputs of nutrients and labile (easily broken apart, T. Visel) organics.  Once the critical organic loading rate is exceeded, stage III taxa are locally eliminated, and organic enrichment species (sensu, Pearson and Rosenberg, (1978) dominate.  This may be related to the accumulation of antibiotic decomposition products, (Bades, 1954) low dissolved oxygen (Rhoads and Morse 1971) sulphides, or a combination of these factors.  As described earlier, the influence of stage 1 seres on nutrient cycling (these could be described as composting or reworking organisms – T. Visel) and aeration of the sediment column may be very limited.  Hence, sulphate reduction and methanogenesis predominate over oxidation metabolism.  These metabolites sulphides, ammonium, and methane contribute further to bottom water oxygen demands as they diffuse into the water column.

The loss of a stage III sere (aging series) from an area and its replacement by a state 1 sere may be expected to be accompanied by a major change in both the depth and rate of biogenic processing of bottom sediments.   Evidence of such a retrograde succession is an early warning sign of the potential for developing hypoxic or anoxic conditions in the near future."   

This excerpt describes conditions that can be measured by an increasing depth of sapropels.  Biogenic processing is bacterial (and fungal and yeasts) breakdown of organic tissue.  Low oxygen restricts "normal" or accepted rates of bacterial reduction and assists in the transition of aerobic life that can live without oxygen."


Appendix #5

FAO TRAINING MANUAL ON BREEDING AND CULTURE OF SCALLOP AND SEA CUCUMBER IN CHINA

CHAPTER 1
STRUCTURE AND BIOLOGY OF SCALLOPS

1.   Argopecten irradians, the bay scallop, has a wide geographical distribution along the Atlantic and Gulf coasts of the United States. After being transplanted into China in 1982, the bay scallop gradually became one of the dominant species of scallops cultivated in China.
2.   Furthermore, heavier mortality occurs with higher culture density and bigger sized individuals.
3.   An unsuitably high culture density may be the main cause of mortality. The reasons are: (1) the scallops cannot obtain sufficient food; (2) a greater amount of metabolic waste is produced, the decomposition of which will consume great quantity of dissolved oxygen; (3) the products of decomposition, especially sulphide, are toxic to scallops; some experiments have shown that when the sulphide concentration reaches 0.3 ppm, the filtration rate of scallop is reduced by about 30 %, and at 0.7 ppm, feeding and respiration stop; and (4) the weak individuals in a crowded and adverse environment are susceptible to disease.
4.   Other important factors that cause mortality are high temperature and high density of fouling organisms.
Oceanology of China Seas – Volume 1, Edited by Zhau Di – Kluver Academic publishers

"The decomposition of fecal pellets of parent scallops, food debris and dead scallops by enculture bacteria as well as metabolic wastes may produce toxic ammonia. When waste materials are sedimented and oxygen in the tank is exhausted, toxic hydrogen sulfide is produced. Aeration serves to replenish oxygen in the water resulting in converting hydrogen sulfide into hydro-sulfate and at the same time restricts the growth of anaerobic bacteria, thereby reducing the production of toxic ammonia. Lowering the pH of the water can have a diluting effect on toxic ammonia."



Appendix #6

Shellfishers on Cape Cod Notice Habitat Succession


Shellfishers on Cape Cod frequently noted that once firm bottoms, which were good clam bottoms, had turned soft filled with dead clams (comments to T. Visel, 1981-1983).  Inlets on Cape Cod were beginning to close and become stagnant or poorly flushed.  Those salt ponds had a deepening deposit of organic matter, an ooze or soft bottom.  In April 1999, Sandra Macfarlane wrote a report for my old employer The Barnstable County's Cape Cod Cooperative Extension Service titled "Bay Scallops in Massachusetts Waters: A Review of the Fishery and Prospects for Future Enhancement and Aquaculture," 27 pages.  On page 16, Macfarlane notes that a survey contained components now associated with warming waters, soil conditions, increased algal blooms and tidal choking – closing of inlets.  From page 16 is found the following:

"Many respondents reported a change in sediment from hard to soft (44%) but few reported a change from soft to hard (4%).  Respondents also noticed increased phytoplankton blooms (44%) and an increase in motor boat activity (87%) with a concomitant increase in boat size (61%).  Inlet dynamics have changed according to a number of respondents where 57% is a result of natural occurrence, 22% from dredged channels and 9% from jetties, seawalls or other structures."

The transition from "hard" to "soft" bottoms would be noticed in southern New England, just not on Cape Cod.