AMER. ZOOL., 37:612-620 (1997)
Bacteria, Dissolved Organics and Oxygen Consumption in
Salinity Stratified Chesapeake Bay, an Anoxia Paradigm1
ROBERT B. JONAS
2
Department of Biology George Mason University,
4400 University Drive, Fairfax, Virginia, VA 22030
SYNOPSIS. Chesapeake Bay is a bacterially dominated ecosystem driven, at least
dissolved organics. Bacteriounder summer conditions, by high levels of labile
are 1exceptionally
abundant (20 x 109 cells liter'1) and productive (7 x
plankton
9
1
10 cells liter" d" ), and their biomass can equal or exceed 60% of phytoplankton
biomass. In the salinity stratified Chesapeake Bay bacterioplankton account for
60-100% of planktonic oxygen consumption, potentially driving the Bay to anoxia
in days to weeks. Sulfide, released from sediments by sulfate lreducing bacteria,
chemically consumes oxygen at rates up to 9 mg O2 liter ' d maintaining the
oxygen deficit. The organic matter driving this oxygen demand in the summer
season is functionally dissolved. Dissolved organics, measured as biochemical oxygen demand, account for about 60% of microbially labile organics throughout
the water column and 80% (sometimes 100%) in the subpycnoclinal water. Field
studies suggest that reduced oyster stocks in Chesapeake Bay may be a major
factor in the shift to this bacterially dominated trophic structure.
INTRODUCTION
Although the importance of bacterial
communities in ecosystem function is not
in dispute, bacterial distributions and metabolism of organic matter are rarely considered directly in zoological investigations.
The reason for considering these topics here
is that there is now a large body of evidence
indicating that, in some aquatic ecosystems,
bacterial processes have changed, and now
control important aspects of the physicochemical environment in which the macrobiota live. Therefore, investigating the distributions and adaptations of the macrobiota
must begin with an understanding of bacterial dynamics in these systems.
The goal of this paper is to present evidence that dissolved organic matter and
bacterial metabolism of that organic matter
are, quantitatively, major components of
aquatic ecosystems, including salinity stratified Chesapeake Bay, the nation's largest
estuary. It is a mesotrophic ecosystem
which suffers from seasonal hypoxia and
' From the Symposium Molecules to Mudflats presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 26-30 December
1995, at Washington, D.C.
2
E-mail: [email protected]
anoxia, produced directly, and maintained
directly and indirectly, by bacterial activity
(Jonas and Tuttle, 1990; Jonas, 1992). Consideration of data from Chesapeake Bay indicate that a modified trophic paradigm is
needed. Rather than the classical trophic
pyramid, the high concentrations of dissolved organics and extreme abundance of
metabolically active bacteria imply that a
"teardrop" shape might better represent
this portion of the trophic model or paradigm (Fig. 1). In grammar the term "paradigm" is an example of a conjugation giving ALL the inflections of a word. In the
Chesapeake Bay and, perhaps other estuaries, the critical role of bacteria should be
recognized as one important "inflection" of
ecosystem structure and function.
Low oxygen conditions in Chesapeake
Bay are not new. Sale and Skinner (1917)
(Fig. 2A) found deep water oxygen concentrations in the lower Potomac River to be
only 20% of saturation in the summer of
1912. Newcomb and Home (1938) reported
"true" anoxia in the Bay's mainstem during
1936. Salinity stratification, high salt concentrations in the deep water, provides the
physical environment which allows oxygen
depletion in the Bay (Boicourt, 1992), but
anoxia events were quite rare and transient
612
BACTERIA AND ANOXIA IN CHESAPEAKE BAY
Trophic Models
Grazer Detrital
PYRAMID
TROPHIC
Microbial
TEARDROP
FIG. 1. Trophic models including the classic pyramid
representing grazer/detrital food webs and the proposed teardrop shape representing a bacterially dominated aquatic ecosystem. The wider base of the latter
indicates the quantitative importance of dissolved organic matter (DOM) and bacteria.
until the 1970s, even in years when the water column was highly stratified (EPA,
1982). During the past two decades summer-long anoxia has occurred almost yearly, affecting the mainstem, from north of
Annapolis, Maryland to an area south of the
Potomac River, and the lower reaches of the
subestuaries. The damage which can be
done by this situation is evident from the
seicching event documented in 1984 (Fig.
3) (Malone et al, 1986). Anoxic water, containing toxic hydrogen sulfide (H 2 S),
"sloshed" to the western side of the Bay
mainstem reaching depths as shallow as 2
meters and covering nearly all of the benthos.
It is generally understood that heterotrophic microbial processes led to the oxygen
depletion. However, very little was known
about the nature of the microbial community involved, its rate of metabolism or the
organic matter fuelling the oxygen consumption. Therefore, extensive investigations were conducted to probe the relationships among nutrient enrichment, phytoplankton production and bacterioplankton
distributions and metabolism (Tuttle et al,
1987ft Smith et al, 1992).
EXPERIMENTAL APPROACH
It is beyond the scope of this summary
to describe these studies in detail. The basic
approach was to conduct repeated seasonal
cruises on the Chesapeake Bay occupying
multiple stations along cross-bay transects
located within the region affected by an-
613
oxia. At each station, vertical profiles of nutrient conditions, phytoplankton and bacterial distributions and activities, and organic
carbon distributions were determined. In
the case of the bacteria and organics, measurements were made of bacterial abundance, production, and metabolism of selected organic carbon compounds. Biochemical oxygen demand (BOD) (measured
by oxygen concentration changes during 5day incubations in dark bottles) and "dissolved" BOD (filterable organics passing
Gelman Type A/E glass fiber filters under
5 in. Hg vacuum) were measured to estimate the amount of bacterially available organic matter. Concentrations of reducing
sugars (reported as glucose) and amino acids were assayed chemically (Bell et al.,
1988; Jonas et al, 1988a; Jonas and Tuttle,
1990; Jonas, 1992).
RESULTS AND DISCUSSION
Figure 2B is a typical vertical profile of
water quality parameters under summer
conditions in the mainstem of Chesapeake
Bay and in the lower reaches of the rivers
feeding the Bay. Although there is little
change in temperature with depth, salinity
increases dramatically in the mid-water,
usually at depths of about 9 to 13 meters.
The resulting rapid increase in density of
the water (pycnocline) physically isolates
and limits reaeration of the deep water. Biological and/or chemical oxygen demand
drives oxygen concentrations from near saturation to zero (anoxia) over a vertical distance of only about 2 meters. Bacterially
produced, H2S diffuses upward from its
source in the sediments (Tuttle et al.,
1987a; Tuttle et al, 1987c; Divan and Tuttle, 1988). Although the H2S concentrations
shown in Figure 2B are some of the highest
found in Chesapeake Bay water, in other
locations H2S concentrations routinely
range around 10 (xM or less.
Bacterial abundance and production
The simple fact that heterotrophic processes consume dissolved oxygen was
known. However, the physical location of
oxygen consumption could be either the
sediments or the water column (or both)
(Kemp et al, 1987), and the biological con-
614
ROBERT B. JONAS
POTOMAC RIVER
WASHINGTON TO POINT LOOKOUT
120
SALE AND SKINNER, 1912 DATA
110
100
Upstream
90
80
70
3
60
50
O
40
d
30
20
10
0
1
2
3
4
6
6
7
8
9 10 11 12 13 14 15 16 17 18 19 20 21
STATIONS ARRANGED DOWNSTREAM
SURFACE
^m BOTTOM
Potomac River, Piney Point
TEMP (oC), SAL (ppt), DO (mg/l), pH
0
B
5
10
15
20
25
30
£10
TEMP (oC)
Q_
LU 15
SAL^ppt)
DO (rng/l)
PH
20
Sulfidg (uM)
25
20
40
60
80
100
Sulfide (uM)
FIG. 2. A. Dissolved oxygen concentrations in surface and bottom water of the Potomac River from Washington
D.C. to the river mouth at the Chesapeake Bay in 1912. B. A typical vertical profile of salinity, temperature,
dissolved oxygen, pH and hydrogen sulfide in the lower Potomac River near Piney Point in the 1980s.
sumption process was not clearly elucidated.
Our investigations (Tuttle et al, 1987a;
TAittle et al, 1987&; Jonas, 1992; Smith et
al, 1992) of bacterial distributions and ac-
tivity revealed unprecedentedly high bacterial abundances (Fig. 4A) and secondary
production (Fig. 4B). During summer, bacterial abundances, assessed by direct microscopic enumeration of acridine orange
615
BACTERIA AND ANOXIA IN CHESAPEAKE BAY
Aug 20, 1984
Station
3
1 2
4
5
Aug 23, 1984
1
Station
3
2
45
East
12
0
12
4
16
DISTANCE (Km)
FIG. 3. Cross-Chesapeake Bay depth profile of water density (sigma-t) and dissolved oxygen on 20 August
and 23 August, 1984. On 20 August wind blew strongly from the northwest pushing surface water to the east
which caused tilting of the deep layers toward the west. During this period anoxic water covered both flanks of
the Bay to depths as shallow as 2 meters (west).
20
o
c
15
ID
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J ,
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8
(0
4
"col
<5 ~ 6
m
2
50
100
200
150
250
Julian Days
Euphotic
Midwater
Subpycnocline
FIG. 4. Seasonal distributions of depth integrated mean (A) bacterial abundance and (B) bacterial production
in three depth zones along a cross-Chesapeake Bay transect located near the mouth of the Potomac River. Open
triangles represent sampling cruises.
616
ROBERT B. JONAS
stained cells (Hobbie et al., 1977), routinely
rise to 10-20 X 109 cells liter"1 with occasional values as high as 50 X 109 liter"1.
These are the highest sustained bacterial
abundances reported from any estuary.
Usual values range from about 1-7 X 109
cells liter"1.
There was also a repeating seasonal pattern of bacterial abundance changes (Ducklow et al, 1988; Jonas, 1992). Depth integrated abundance (Fig. 4A) along a crossbay transect south of the Potomac River, in
the Virginia portion of the mainstem which
suffers from anoxia, are representative of
the entire mesohaline Chesapeake. Typically, abundances throughout the water column are a few billion liter"' in early spring,
and rise through April and May, tracking,
with a time lag of one to two weeks, the
spring phytoplankton bloom (Allen et al.,
1996). Subsequently, abundances decline
following the phytoplankton population
crash, only to rise to very high levels in
July and August, in the absence of high
phytoplankton populations.
Our multiyear studies show that the large
majority of the bacteria in Chesapeake Bay
are "free-living" and very small; more than
90% are less than 1 (im long. In other estuaries, more than half of the bacteria
would be attached to detritus particles. It is
generally believed that "particle association" helps bacteria efficiently "find" food.
Therefore, the free-living habit of bacteria
in Chesapeake Bay suggested that they easily find food without being attached to particles and that there may be high concentrations of microbially labile organics available to them.
Although the seasonal pattern of bacterial
production (Fig. 4B), assayed by tritiated
thymidine incorporation, does not correlate
well with bacterial abundance, it too is repetitive on an interannual basis, and summer values are very high. Seasonal maximum of about 1010 cells produced liter"1 d~'
occur in late May and June. Bacterial production in the euphotic zone is often 30%
of phytoplankton production and sometimes
reaches value 100% or more of phytoplankton production (Ducklow et al., 1988; Jonas, 1992). Usual bacterial production in other estuaries would be 20% or less of phy-
toplankton production (Ducklow et al.,
1988). Assuming that bacterial abundance
is constant on a day to day basis, these production values indicate that the bacterial
community "turns over" completely once
every 0.5 to 2 days.
Oxygen consumption
There are two bacterially driven, water
column oxygen consumption process which
can account for oxygen depletion in the
Bay:
1) direct aerobic respiration:
CH2 + O2 -> CO2 + H2O
2) oxidation of H2S which is a by-product of anaerobic respiration
2[CH2O] + SO2" -» S2" + 2CO2 + 2H2O
S2" + 2O2 -» SO|"
Directly measured oxygen consumption
rates in Chesapeake Bay, estimated from
short-term oxygen concentration changes in
sealed, dark bottles, are about 1-1.5 mg O2
liter"1 d"1 (Turtle et al., 1987a). Calculated
O 2 consumption rates based on measured
bacterial abundances and biomass specific
oxygen consumption rates are also about 1—
1.5 mg O2 liter"1 d"1. Oxygen consumption
correlates strongly (r2 = 0.90) with bacterial abundance over several years. Experimentally, oxygen consumption is accounted
for primarily (70-100%) by organisms
smaller than 3 u.m (Sampou et al., 1988).
It is seems likely that water column oxygen
consumption is primarily due to bacterial
processes in the water column when free
molecular oxygen is available. Thus, bacteria consume the oxygen, and, assuming
oxygen saturation of about 7 mg liter"1 they
can drive the dissolved oxygen to zero in
about 5-7 days. Once anoxia occurs, H2S
can diffuse from the sediment (evidence indicates that little water column sulfide production occurs (Tuttle et al., 1987a, c) into
the overlying water and act as a chemical
oxygen demand and maintain anoxic conditions.
Microbially available organic matter
There must be a major source of organic
matter to support the bacterial community
617
BACTERIA AND ANOXIA IN CHESAPEAKE BAY
2.0
5.0
A Total BOD
K
M
/A
' V
4.0 "
A
1.5
/
30
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r
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f-
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2
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0.4
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0.2 W
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200
150
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Julian Days
Euphotic
Midwater
Subpycnocline
FIG. 5. Seasonal distributions of depth integrated mean (A) total biochemical oxygen demand (BOD) and (B)
dissolved biochemical oxygen demand (dissolved BOD) in three depth zones along a cross-Chesapeake Bay
transect located near the mouth of the Potomac River. Open triangles represent sampling cruises.
in Chesapeake Bay. Although the Bay is enriched in nutrients (mesotrophic), the phytoplankton biomass is usually not exceptional (Smith et al, 1992). This condition
along with the high percentage of free-living bacteria suggested the possible importance of dissolved organic matter. On average in Chesapeake Bay microbially labile
organic matter, measured as BOD, ranged
seasonally from about 1-4 mg O 2 liter" 1
(Fig. 5A), with the highest springtime values occurring in the bottom water and highest summer values in the surface. During
phytoplankton blooms, surface BODs often
exceed 7 mg O 2 liter" 1 . Dissolved BOD was
surprisingly high, ranging from about 0.5 to
2 mg O 2 liter" 1 (Fig. 5B) with peaks in late
spring and summer. Dissolved BOD averaged about 50% of total BOD through
spring and summer, and in the deep water,
beneath the pycnocline, averaged 60% or
more of the total (Fig. 6). At some stations
dissolved BOD made up 100% of the microbially labile organic matter.
In spring, bacterial abundance (r = 0.56)
and production (r = 0.77) correlate significantly with particulate BOD, but in summer they do not (r = 0.27, r = 0.16 respectively). In summer, bacterial abundance
(/• = 0.62) and production (r = 0.54) correlate significantly with dissolved BOD, but
they do not in spring (r = 0.12, r = 0.37
respectively). It appears that the "excessive" bacteria in Chesapeake Bay during
summer rely on a large pool of dissolved
organic matter which is likely produced in
situ by the phytoplankton (Zieman and
Macko, 1988; Jonas, 1992).
Data indicate that average phytoplankton
extracellular release of dissolved organic
matter in mesotrophic systems ranges from
21 to 3 8 % with exceptional values of 60%
(Chrost, 1983; Bell and Kuparinen, 1984;
Kato and Stabel, 1984; Rai, 1984). This reGANSERUBRARY
MJLLEFGVILLE LfrliVERSnY
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618
ROBERT B. JONAS
FIG. 6. Seasonal variation in the vertical distribution of the percentage of total biochemical oxygen demand
represented by dissolved (filterable) biochemical oxygen demand (FBOD) in Chesapeake Bay. Each time point
(non-scaled axis) represents a sampling cruise.
lease may occur as a result of active excretion, leakage, sloppy feeding by herbivores,
and cell lysis. On a percentage basis it appears that phytoplankton extracellular release is greatest in mesotrophic systems
compared with oligotophic and eutrophic
(including hypertrophic) aquatic systems
which average about 20% and 10% respectively (Munster and Chrost, 1990).
Free dissolved reducing sugars, expressed as glucose, and free dissolved amino acids were present in very high concentrations in Chesapeake Bay water (Jonas et
al, 1988a, b). We found that during summer glucose averaged about 500—800 nM
and often peaked in concentration (1200
nM) at the pycnocline. Free amino acids averaged about 200 nM with dramatic peaks
exceeding 1000 nM at the pycnocline. Glucose and amino acid concentrations alone
account for about 60-70% of the BOD near
the pycnocline, although they represent
only about 30% of total BOD in the surface
waters.
The remaining dissolved organic matter
has not been accounted for in Chesapeake
Bay, but the work of Munster and Chr6st
(1990) suggests that glycolic acid may be
the single most abundant dissolved compound derived from algal release. They reported glycolic acid concentrations as high
as 4,000 nM. Our investigations did not include assessments of this compound. Beneath the pycnocline, in Chesapeake Bay,
fermentation end-products may also be important. In our studies, although we did not
measure the concentrations, acetate turnover was extremely high (more than 70%
of the acetate pool utilized per hour) just
below the pycnocline (Bell et al, 1988).
Glucose and amino acid turnover rates
were generally high during spring and summer, ranging from about 10 to 50% per hour
for glucose and 4 to 20% per hour for amino acids (Tuttle et al, \9%lb; Bell et al,
1988; Jonas et al, 1988a; Jonas, 1992).
Turnover rates increased with increasing
concentrations of these two types of organics, indicating that there is an active microbial community poised to take advantage of
available dissolved organics.
SUMMARY
The high levels of bacterial activity in
Chesapeake Bay indicate that there may
have been a major shift in the trophic structure of this ecosystem. The Bay appears to
have shifted from a metazoan chain in
which the primary production was grazed
by herbivores such as zooplankton and benthic filter feeders, to a microbially dominated system in which large amounts of primary production is now consumed by bacteria. It has been speculated that reductions
in the biomass of benthic filter feeders, especially oysters, is one of the causes of this
trophic shift (Newell, 1988). Filter feeder
abundance declined due to overharvesting,
BACTERIA AND ANOXIA IN CHESAPEAKE BAY
poor water quality and/or disease. This decline could lead to increased phytoplankton
abundance and increased concentrations of
dissolved, microbially available organics,
which subsequently support high levels of
bacterial abundance. Aerobic bacteria consume large amounts of organic matter
which leads to hypoxia and, ultimately, anoxia in the water column. While hypoxia
itself can be devastating to the macrobiota,
anoxia in the water column can initiate a
sequence of events (e.g., anaerobic respiration) which results in overtly toxic conditions (high H2S concentrations) and perpetuates itself through chemical oxygen demand.
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