AEROBIC DECOMPOSITION
OF SEDIMENT
AND
DETRITUS AS A FUNCTION
OF PARTICLE
SURFACE
AREA AND ORGANIC CONTENT
Bawy T. Hargrad
Freshwater
Biological
Laboratory,
The University
of Copenhagen,
Hillergd,
Denmark
ABSTRACT
Oxygen uptake by microbial populations
on mud, sand, and various types of detritus was
measured in short-term
experiments
in aerated water at 20C. Sample size had no effect
on oxygen consumption
per unit weight, but stirring increased uptake.
A 2% Formalin
solution completely
stopped biological
uptake of oxygen by microorganisms
on sand and
detritus; lake muds showed various degrees of chemical uptake of oxygen.
Microorganisms
on dead Phrugmites leaves consumed oxygen at an increasing rate during
the first few days of decomposition,
followed by a decline to a rate comparable to uptake
by freshly collected detritus.
Limnaea feces initially
consumed oxygen three times more
rapidly than detritus, but after 5 days the rates were equal.
Detritus consumed up to three orders of magnitude more oxygen per dry weight than
sand; uptake rates were inversely related to particle diameter.
The logarithm
of oxygen
uptake was directly related to the logarithm of particle organic content. Particulate
oxygen
uptake in this and previous studies fell between 0.1 and 10 mg 02 (g organic matter)-l hr-l,
a rate inversely related to particle diameter.
Oxygen uptake per unit weight by particles
of ashed mud and sand exposed for 24 hr to decomposing
detritus in a nutrient solution
and transferred
to fresh solution was inversely related to particle size and similar to rates
measured with freshly collected samples. On an areal basis all particles consumed between
0.01 and 1.0 x lo-’ mg O2 cm-l hr-I.
The negative linear correlation
on logarithmic
axes of surface area, organic carbon and
nitrogen and bacterial plate counts with sediment particle size is similar to that observed
for measures of oxygen uptake. Bacteria cover only a few percent of particle surfaces. This
may result in the narrow range of measures of microbial
community
respiration
on an
areal basis.
INTRODUCTION
Aquatic sediments and detritus consume
oxygen when stirred in aerated water, The
oxygen uptake is an integrative measure
of all oxidative processes occurring in the
sample, both chemical
and biological.
Reducing substances are usually rapidly
oxidized. Respiration of the organisms associated with particles is probably primarily bacterial, although algae, protozoa,
and fungi may also contribute.
Whatever
populations are involved, measurements of
oxygen uptake reflect the metabolism of
communities of microorganisms
involved
in the decomposition of natural substrates.
No measure is provided, however, of anoxic microbial decomposition.
Many workers have measured rates of
l Present address:
Fisheries Research Board of
Canada, Marinc Ecology Laboratory,
Bedford Institute of Oceanography,
Dartmouth,
Nova Scotia,
LIMNOLOGY
AND
OCEANOGRAPHY
583
oxygen uptake by detritus,
mud, and
sand sediments. Waksman and Hotchkiss
( 1938)) Teal ( 1962), and Rybak ( 1969)
suggested that oxygen uptake is related to
the organic matter available for decomposition; Odum and de la Cruz (1967) and
Fenchcl (1970) d cmonstrated an invcrsc
relation between detritus particle size and
oxygen consumption.
Chemical oxidation
of reduced subsurface sediment may also
be related to the concentration of reduced
substances (Gardner and Let 1965; Hargrave 1972).
Teal (1962) and Odum and de la Cruz
( 1967) found approximately
similar rates
of oxygen consumption by Spartina detritus. Thalassia decays much faster than
does Spartina (Wood et al. 1969)) yet oxygen uptake by detritus from these plants,
freshly collected or artificially prepared, is
similar ( Fenchel 1970). Lake Esrom scdimcnts consume oxygen at rates similar to
JULY
1972,
v.
17( 4)
584
BARRY
T.
those observed with salt marsh mud (Hargrave 1972).
I here compare rates of oxygen uptake
by sediment and detritus particles of different sizes and organic content, These
results, combined with previous measurcments, show an inverse relation between
particle size and oxygen consumption. The
importance of surface area and organic
content is examined by calculating oxygen
uptake of natural and recolonized particles on a surface area basis. A possible
mechanism causing similarities and differences in rates of sediment oxygen consump tion is suggested.
I gratefully acknowledge a NATO Science Fellowship provided by The National
Research Council of Canada, Professors E.
Stecmann Nielsen and T. Fcnchel kindly
read the manuscript
and offered comments. Mr. S. Bordon calculated the regression lines.
MATERIALS
AND
METI-IODS
Sediment and detritus from freshwater
sources were collected from eutrophic
Lake Esrom and Frederiksborg
Castle
Lake, from the humic-acid brown-water
Store Grib Lake, all located in northern
Zealand (Denmark) (Berg 1938), and from
Grane Lang Lake, an oligotrophic lake in
Jutland (Whiteside 1970). Other samples
were taken from Hclsing@r, Kronborg, and
Julebaek beaches along the northern @resund near Helsinger ( Fenchel 1969).
Either a Kajak corer (Brinkhurst
et al.
1969) or a glass cylinder pushed by hand
into shallow sand sediment was used to
take undisturbed cores of mud and sand.
In the laboratory, samples of mud and fine
sand sediment wcrc taken from the surface
of the cores by pipette, mixed, and drained
on filter paper. About 0.1 g wet wt was
removed from the filter paper with a
spatula and added to 28-ml Pyrex BOD
bottles filled by siphon with filtered aerated water from the collecting area. Large
pebbles, with a total weight of up to 5 g,
were added to bottles with forceps. Detritus collected by hand from beach margins
I-IARGRAVE
was used immediately.
Disks (l-cm diam)
were cut from larger pieces of decaying
vegetation with a cork borer and lo-20
mg (dry wt) were placed in bottles. Incubations lasted l-2 hr in the dark at 2OC,
and bottles were rotated (4 rpm) on their
long axis to prevent oxygen depletion
around sedimented particles. All experiments were carried out during summer
and early fall when field temperatures
ranged between 10 and 22C.
A buffered (pH 6.8) solution of 2% Formalin was used to fill some BOD bottles.
ZoBell and Brown (1944) found that a
0.25% Formalin solution stopped bacterial
respiration, so oxygen consumed by particlcs in this solution was assumed to be due
to chemical uptake. Additional blank bottles corrected for small amounts of oxygen
uptake by the Formalin.
Dissolved oxygen was measured by a
micro-Winkler
technique (Fox and Wingfield 1938) with samples taken in 5-ml
syringes; a solution of 1% NaN3 was added
to the NaI solution to prevent interference
from reduced substances. Syringe samples
of supernatant were taken after settling
of particles. Mud particles, in particular,
appear to bind the iodide liberated during the Winkler reaction and thus reduce
the apparent oxygen concentration.
Formalin soIutions were titrated slowly over
10 min for accurate end-point determinations. Measurements of dissolved oxygen
were accurate to at least 0.1 mg/liter.
Changes as smalI as 1% of total oxygen
present could be measured; changes were
usually much greater, but concentrations
were never reduced more than 30%. Corrections were made for volume displacemcnt throughout.
Mud and detritus were filtered onto preashed and preweighcd
glass-fiber filters,
dried ( 8OC for 24 hr ), and weighed. Sand
grains and pebbles were dried in preOrganic matter was
weighed crucibles.
determined by loss on ignition at 550C for
3 hr; carbonate dissociation is avoided at
this temperature if ashing times are not
long (Rybak 1969). Particle size (mean
value of greatest dimension of randomly
DECOMPOSITION
OF SEDIMENT
chosen particles) of sand grains was determined by microscopic examination; at least
100 were examined when their diameter
was less than 500 p. All pebbles greater
than l-mm diameter in the bottles were
measured and the mean diameter dctermined, Mud sediments consisted entirely
of silt and amorphous organic debris that,
with gentle agitation, passed through a
nylon screen with 100-p-mesh openings
but clogged screens of 20 p; an average
particle diameter of 50 p was assumed.
The detritus from decaying vegetation,
when not cut with a cork borer, was measured wet on graph paper or under a
binocular microscope.
Fecal pellets were collected from three
common benthic invertebrates in Lake Esrom. Adult Ilyoclrilus hummoniensis ( Oligochaeta) and fourth instar Chironomus
anthracinus (Diptera) larvae were held in
freshly collected profundal lake mud, and
fecal pellets were collected from petri
dishes in which several animals had been
held overnight.
Limnaea palustris ( Mollusca ) , collected with decaying Phragmites communis, browses epiphytic material
and produces abundant feces. All fecal
pellets were kept in gently aerated lake
water when not used within a few hours,
Rates of oxygen consumption per unit
weight were compared on a surface area
basis by dividing rates of oxygen uptake
by the number of square centimeters of
sediment. Area was calculated for detritus
particles larger than 1 mm before drying
by doubling that traced on graph paper.
Values for mud and detritus with a particle diameter less than 1 mm were taken
from Fenchel’s (1970) estimate of total
surface area per gram dry weight of Thalassia detritus. Sand grain and pebble surface area was estimated from a relation
between mean sand grain size and “internal surface” arca derived by Fenchcl
( 1969), based on 10 cm3 of sample and
the assumption that sand grains were
spherical. If the specific gravity of sand
(quartz) is assumed to be 1.6 (Kaye and
Laby 1956), then the surface area per
gram dry weight for a given sand grain
585
AND DETRITUS
diameter is Fenchel’s internal surface area
divided by 16.
Recolonization
expcrimcnts
were on
mud, sand, and pebbles from Lake Esrom
sterilized by ashing at 550C for 3 hr. A
small piece of decomposing Phragmites
leaf in a solution of 1% each of glucose,
peptone, and K&P04
and mud-water extract (1 kg of wet profundal mud autoclaved with 1 liter of Lake Esrom water)
was used for inoculum, with controls of
sterilized particles in autoclavcd lake watcr without detritus. After 24 hr of aeration, control and inoculated particles were
rinsed and placed in freshly filtered water,
and oxygen uptake was measured.
RESULTS
Experimental
variables
Lake Esrom mud between 1 and 20 mg
( dry wt ) per bottle gave no significantly
different rates of oxygen uptake per gram
dry weight. Eight samples of surface sediment taken from four profundal mud cores
during June consumed 0.22 * 0.04 mg 02
g-l hr-l regardless of sample size. Samples
of sand grains (250-p diam), from a beach
surface in Lake Esrom, of dry weights
up to 1 g showed similar reproducibility
(220%). Two replicate samples were then
used for each determination and the mean
value recorded. Short incubations, l-2 hr,
ensured sufficient oxygen yet gave measurable changes in concentration.
The
rapid oxygen uptake by some sediment
and detritus particles necessitated agitation of samples. Profundal mud from Lake
Esrom consumed 0.32 mg 02 g-l hr.-l when
bottles were slowly rotated and 0.08 when
standing. Oxygen uptake of beach sand
decreased by 15% when it was not stirred.
Relative importance of chemical
and biological oxidation
Oxygen uptake by sand and detritus
from beaches was always completely
stopped by 2% Formalin; oxygen uptake
by subsurface sediment from below 2 cm
in cores from Store Grib Lake and Lake
Esrom was unaffected by Formalin treat-
586
BARRY T. HARGRAVE
TABLE 1. Effect of Formalin treatment (+ = with, - = without)
on oxygen uptake by surface (upper 5 mm) mud from four Danish lakes at various times of the year. All values are means of at least
two separate determinations
-
+
(mg 0, g-1 hr-1)
Esrom
15 Jun
13 Nov
15 Dee
0.75
1.48
1.14
0.44
0.87
0.35
Oxygen uptake
by chemical
Biological
oxidation
respiration
(mg
0, g-1 hr-1)
(%I
59
59
31
0.31
0.61
0.79
Sediment
org matter
(%I
mg 0,
(g org
matter)-1 hr-1
39.6
40.0
39.9
0.78
1.52
1.98
x
Store Grib
5 Sep
Freclcriksborg
22 Sep
Grant Lang
15 Mar
1.43
0.74
0.48
65
0.26
72.0
0.36
1.34
0.73
54
0.61
45.0
1.36
0.10
0.01
10
0.09
21.3
0.43
Castle
ment, indicating
that oxidative processes
were chemical, Surface muds (upper 5 mm
as taken by pipette) from various lakes,
however, showed varying degrees of sensitivity to poisoning (Table 1). Oxygen was
present ( 3-5 mg/liter ) over all sampled
cores. Data from Lake Esrom show considerable seasonal variation in total oxygen
uptake and the amount susceptible to Formalin poisoning.
Particle size and organic content
Oxygen uptake by sand grains, detritus
particles, and mud sediments was different per unit weight and each varied on the
basis of mean particle diameter (Fig. 1).
With the logarithmic
transformation
of
both axes, Fig. 1 reveals a linear, inverse
relation between particle diameter and oxygen uptake. Values for mud were omitted
from the regression calculations because of
the inaccurate estimation of particle size.
Oxygen uptake for a given particle diameter was two to three orders of magnitude
higher for detritus than for sand. Sand
grains and pebbles contained less than 1%
organic matter while mud and detritus
particles contained 40-90% organic matter.
After logarithmic transformations,
oxygen
uptake was linearly related to organic content (Fig. 2).
The effect of differences in percentage
of organic matter in various types of scdiment was standardized by expressing oxygen uptake on an ash-free weight basis.
In sand and detritus this measure reflects
the metabolic activity of communities of
microorganisms
since these substrates
showed no chemical oxidation. Mud particles did undergo chemical oxygen uptake
and this has been subtracted in the calculations of biological respiration in Table
1. The range of values of oxygen uptake
by various particles was reduced by these
calculations, and the effect of particle size
was enhanced (Fig. 3). Oxygen uptake by
all material fell within the range [O.l-10.0
mg 02 (g org matter)-l hr-l] observed for
detritus ( Fig. 1) largely because values
for oxygen uptake by sand grain communities, when expressed on an ash-free basis, were raised. Although differences are
large, organic matter in various muds was
oxidized at much lower rates than detritus
particles of similar size.
Stage of decomposition
Fresh snail fecal pellets (about 0.5-mm
diam and 2 mm long) contained 80-90%
organic matter. This always increased as
they aged, probably from organic matter
removed from solution by microorganisms
colonizing their surfaces, although it could
also result from leaching of inorganic salts.
DECOhXTi’OSITION
OF
SEDIMENT
AND
587
DETRITUS
bacteria
sand
,
,
/
/
/
/
/
/
,
,
0
0
0
-4 -I 0 8c,““I
1 8 I II”11 1 18““‘I
’ “A?
2
3
0
1
. x
4
loglo
particle
diameter
(I-r)
FIG. 1. Relation between mean particle diameter and oxygen uptake per gram dry weight of
sand, mud, and detritus
from various
aquatic
habitats.
Solid circle-detritus
from Lake Esrom shore
(1, mean value for five species of deciduous tree
leaves; 2, unidentified
reed detritus; 3, Phrugmites leaves); solid triangle-invertebrate
feces (lday-old ) ( 1, Limnaea
palustris;
2, Ilyodrilus
hammoniensis.
3, Chironomus
anthrucinus);
solid
square-sand
and unknown seaweed detritus from
Julebaek beach; cross-sand,
detritus,
and mud
from Store Grib Lake; open triangle-Frederiksborg Castle lake mud; point-Grane
Lang Lake
profundal
mud; circled
cross-IIelsinggr
beach
sand; circled
point-Kronborg
beach
pebbles;
open square-sediment
bacteria
(Pseudomonas
spp.) cultured from Lake Esrom surface profundal
mud; open circles-Fenchel
(1970), Thalassia detritus;
squared points-Odum
and de la Cruz
( 1967), Spartina detritus.
y = 1.45 - 0.52 x ( r
Regression lines-detritus:
= 0.65, SE of slope 0.17); sand: y = -0.20 - 0.85
x (r= 0.95, SE of slope 0.07). Slopes are significantly different
from zero (P = 0.05).
Data for
mud, bacteria, Thalassia detritus ( Fenchel 1970))
and Spartina detritus (Odum and de la Cruz 1967)
not included in regression calculations.
Oxygen uptake by microorganisms on fecal pellets used within 6 hr of production
was three times faster than when pellets
were first held for 12 hr (Fig, 4). After 3
FIG. 2. Relation between percent organic matter and oxygen uptake per gram dry weight of
different
particles described in Fig. 1. Regression
line, calculated
omitting bacteria and mud samples, y = -2.15 + 0.90x (r = 0.91, sE of slope
0.075, significant
at P = 0.05).
days the rate of oxygen uptake declined
to 0.55 mg O2 g-1 hr-l, followed by a
slow decrease to 0.25 after holding for 20
days. The decline in oxygen uptake was
accompanied by successions of communities of microorganisms associated with the
fecal material. Ciliates, abundant after the
first day, declined after the fifth. Fungal
hyphac grew rapidly
and changed the
pellets from brown to white within 12 hr.
Phragmites leaves, collected dry from
dead plants in November, were placed in
aerated lake water in the laboratory, Disks
of leaf material tested immediately
contained 82.5% organic matter and consumed
0.22 mg 02 g-l hr-l (Fig. 4). After 3 days
oxygen uptake had increased to 1.0 mg
02 g-l hr-l and leaf material contained
90% organic matter. During the next 2
days there was little change in organic
588
BARRY T. HARGRAVE
c
0 fecal
pellets
“,~~~~~‘, Phragmites
detritus
1.0
0
log ,O particle
0-l)
diameter
FIG. 3. Relation between mean particle diameter and oxygen uptake per gram organic matter
(calculated
from Figs. 1 and 2 ). Symbols as in
Fig. 1. Regression line, calculated omitting mud,
bacteria, and data (line joining points) from Odum
and de la Cruz (1967), y = 2.07 -0.69x
(r = 0.79,
SE of slope 0.10, significant
at P = 0.05).
10
20
Time
30
40
(days)
FIG. 4. Changes in oxygen uptake by Limnuea
feces and Phragmites detritus held at 20C in aerated Lake Esrom water. Samples removed for use
in short-term
experiments
at various times. aDetritus prepared from plant leaves collected dry;
b-detritus
wet and partly
decomposed
when
collected.
Previous measurements
content ( 90.5% ) , but oxygen consumption
fell to the original level. Oxygen uptake
remained constant over the following
34
matter
slowly
inwhile
organic
days,
creased to 98.5%.
In a similar experiment with Phragmites
leaves collected as wet detritus from beside Lake Esrom, oxygen uptake, initially
0.5 mg 02 g-l hr-l, decreased steadily,
while organic matter increased from 94.398.0%. The final constant rate of oxygen
consumption by this material was similar
to those by freshly wetted leaves and
Limnaea feces at the end of the holding
period (Fig. 4). This value (0.25 mg 02
g-1 hrl)
falls within the range observed
for detrital material from other sources
(Fig. 1).
Odum and de la Cruz (1967) and
Fenchel ( 1970) related oxygen uptake to
particle size of Spartina and ThaZussiu detritus. Their results, plotted in Fig, 1, are
of the same magnitude as mine for detritus from different sources.
I have used organic contents of sediment and detrital material reported by
various workers as a basis for comparing
rates of oxygen uptake per unit dry weight
(Fig. 5); sewage particles, artificial stream
periphyton,
aquatic vascular plants, and
aquatic bacteria are included for comparison. When expressed on logarithmic axes,
these data show the same trend and span
the same range as those from this study
(Fig. 2). Odum and de la Cruz ( 1967)
measured both organic content and particle size of decomposing Spartina detritus.
DECOMXPOSITION
OF SEDIUENT
589
AND DETRITUS
m
mg O2 g-’ hr-’
0
percent
m
mg O2 (g organic
organic
matter
m
mg o2 x10-~ cm-* hr-’
matter )-’ hr-’
I
particle
mud
log,o
percent
matter
organic
FIG. 5. Comparison
of organic content and oxygen uptake per gram dry weight for different
types of sediment and detritus, aquatic vascular
plants, periphyton
communities,
and bacterial cells
from previous
studies.
Circles indicate
average
values for measurements at about 20C. Lines represent range of published observations.
l-Johnson
( 1936 ) , resting
marine bacteria;
2-ZoBell
and Stadler (1940),
multiplying
lake
bacteria; 3-Liagino
and Kusnetzov
(cited in ZoBell and Stadler 1940), lake bacteria;
4-Hargrave (1969),
estimated value for lake sediment
bacteria; 5-Gessner
( 1959), various aquatic vascular
plants;
6-McIntire
( 1966))
periphyton
communities
in artificial
streams; 7-Teal
(1962),
Spartina detritus during 4-week decay period; 8Odum and de la Cruz ( 1967), Spartina detritus;
9-Fenchel
( 1970), Thalassia detritus.
N-Water
Pollution
Research Rep. ( 1968),
suspended solids in treated sewage effluent;
llDiSalvo ( 1971), coral reef regenerative
sediment;
12-I&rnerblad
(1930), mean value for 14 Swedish lakes ( assumed 2 g dry wt/flask);
13Miyadi
(cited in ZoBell 1946), lake sediments;
14-Waksman
and Hotchkiss (1938), marine sediments from Woods Hole; 15-Kato
( 1956), marine bottom sediments from the northern
Japan
Sea; 16-Teal
and Kanwisher (1961), surface saltmarsh mud; 17-Gardner
and Let ( 1965), Lake
Mendota sediment (initial 3-day rate); 18-Rybak
diameter
sand
CJI)
pebbles
FIG. 6. Mean oxygen consumption
and organic
content of triplicate
samples of ashed mud, sand,
and pebbles from Lake Esrom after 24 hr of
exposure to Phragmites
detritus in a nutrient-cnriched solution.
Control samples, not exposed to
detritus and nutrients,
contained
no mensurable
organic matter and consumed no oxygen.
Oxygen uptake, on an ash-free basis, follows the trend of my data and falls within
the same order of magnitude when compared with particle size ( Fig. 3).
Particle surface area
All particles considered in this study
consumed between 0.01 and 1.0 x 1O-3 mg
02 cm-2 hr-l with the exception of freshly
produced Limnaea feces (Table 2); oxygen
consumption of fcccs fell to within the
range observed for all other particles
within
3 days. Dctri tus particles consumed more oxygen on an arcal basis than
pebbles, sand, or mud. There was no con-
(1969),
type.
black
clots, Polish lakes of varying
trophic
BARRY T. IIARGRAVE
590
TADLE 2.
Comparison
of mean particle diameter
(p), estimated surface area per gram dry weight
(A), and oxygen uptake per unit surface area (C)
for various types of particles.
Data fur oxygen
uptake per gram (B) from Fig. 1
Particle
and source
Pebbles
Kronborg
beach
Esrom
beach
Sand
Esrom
beach
Helsing@r
Julebmk
A
P
9,000
7,800
5,340
4,000
1,914
1,260
beach
beach
Lake mud
Esrom
Store Crib
Grane Lang
Frederiksborg
Castle
B
1.2 0.00012
1.5 0.00030
1.9 0.00655
2.7 O.OC@70
5.6 0.0012
6.5 0.0011
550
3G6
350
185
248
21.9
31.2
32.0
62.,5
50.0
50
50
50
50
6,000
6,000
6,000
6,000
0.0058
0.0028
0.0046
0.0064
0.0086
0.86
0.74
0.10
1.34
Detritus
Esrom shore debris
0.33
Wet elm leaves
0.18
Phragmites
0.24
E quisetum
0.10
Limnaea feces, fresh 5001 650 3.50
3-day-old
500
650 0.55
Spartina
239 1,050 0.63
(Odum and de
150 1,800 1.62
64 4,200 1.81
la Cruz 1967 )
Thalassia
1,000
420 0.40
400
850 0.60
(Fcnchel
1970)
100 2,500 1.05
C
0.10
0.20
0.2.9
0.26
0.21
0.17
0.26
0.09
0.14
0.10
0.17
0.14
0.12
0.02
0.22
DISCUSSION
0.30
0.42
0.42
0.26
5.38
0.85
0.60
0.90
0.43
0.95
0.71
0.42
sistent relation between oxygen uptake per
square centimeter and particle size.
Recolonization
recolonized pebbles, however, was an order of magnitude higher than that of
freshly collected material. There were few
protozoa in the detritus used for inoculation and thus oxygen consumption probably reflects only bacterial respiration.
No organic matter remained on particles
after ashing, but after 24 hr of exposure
to the nutrient solution and detritus particles a loss on ignition was measured in
all samples (Fig. 6). The percentage organic matter was inversely related to particle size but all particles contained an
order of magnitude less organic matter
than naturally occurring samples of similar type.
Oxygen uptake per gram organic matter,
which ranged from 9-28, was not related
to particle diameter (Fig, 6). Oxygen
consumption
per unit surface area increased with increasing particle size; the
range of values was within that observed
with natural particles (Table 2).
experiments
Previously
ashed pebbles, sand, and
mud, held in sterilized water for 24 hr,
showed no measurable oxygen consumption. After 24 hr of exposure to Phragrnites detritus in an enriched medium, rinsed
samples of mud and sand consumed oxygen at rates inversely related to particle
size and in the range of similarly sized
particles with natural communities of microorganisms (Fig. 6). Oxygen uptake by
The enumeration of microorganisms cannot serve as a measure of their importance
in proccsscs of decomposition.
There may
be no clcarcut relation between numbers
and metabolic rate. The dynamic nature
of microbial populations also makes estimates of population size of limited use;
grazing may stimulate or retard cell division and substrate changes determined by
species succession may continuously affect
probpopulation
size. These limitations
ably account for the lack of correlation
between sediment organic content and
indices ( plate counts) of bacterial biomass
(Cooper et al. 1953; Volkmann and Oppenheimer 1962; Anthony and Hayes 1964).
Also, the amount of total organic matter
in sediment does not indicate its availability to cithcr microorganisms ( Waksman
and Hotchkiss 1938) or invcrtcbratcs (Hargrave 1970a).
Measurement
of oxygen consumption
appears to be a more useful basis for comparing microbial activity in different types
of sediment and detrital material. Hayes
and MacAulay (1959) suggest that oxygen
DECOMPOSITION
OF
SEDIMENT
uptake by mixed mud may represent an
integrative measure of lake productivity.
Although they measured oxygen consumed
by restratified mud-water
systems, there
was a linear relation between oxygen uptake and “lake quality index,” a value
derived from an estimate of fish yield.
Experimental
variables
The interpretation
of oxygen uptake
necessitates standardization of those experimcntal variables which might affect measured rates. For example, Waksman and
Hotchkiss (1938) found shaking to have
no effect, but total oxygen uptake decreased with the amount of sediment per
bottle; I observed opposite effects of shaking and sample size. They left sediment
standing for up to 30 days, stirring it by
hand several times daily.
In long-term
experiments, oxygen dcplction around settled particles would lower the rate of oxygen uptake. The effect would be greater
with larger samples ( Kato 1956). Oxygen
uptake by mud sediments, because of the
small particle size and often high proportion of chemical oxidation ( Table I), may
bc more affected by agitation and size of
sample than sand sediments. The small
range of weights used hcrc (1-28 mg dry
wt/28 ml) may not have been sufficient
to show such an effect.
Sample variability
Changes in rates of oxygen consumption
by sediment and detritus with time can
be expected as easily oxidized substances
disappear. Previous studies with various
types of scdimcnt (Anderson 1939; Kato
1956; Teal and Kanwisher 1961; Gardner
and Lee 1965; Hamilton and Greenfield
1967; Rybak 1969; Fenchel 1969; DiSalvo
1971) all show a time-dependent decrease
in oxygen consumption although the time
scale is different.
The immcdiatc effect
may represent oxygen uptake by reduced
minerals, such as ferrous iron and ferrous
carbonate, and microbial decomposition of
easily oxidized organic substances. Longterm slow rates of oxygen consumption
may bc due to acid-insoluble iron sulfide
AND
DETRITUS
591
minerals (Gardner and Lee 1965) and
slow microbial oxidation of organic matcrial such as lignin and humic complexes.
Whatever the cause of the time-dependent
decrease in oxygen uptake, short-term expcrimcnts give maximum rates of oxygen
consumption, which might reflect rates occurring in nature if samples were taken
from well-aerated areas.
The depth from which a sample is taken
can be important. The variable proportion
of chemical oxidation in lake muds (Lonncrblad 1930 and Table 1) differs from
marinc sand sediment where sterilization
completely stopped oxygen uptake (Waksman and Hotchkiss 1938). The absence
of chemical oxidation of beach sand and
detritus probably results from the welloxygenated
conditions
on wave-washed
beaches where few reducing substances
exist ( Fenchel 1969). Usually, however,
sediments contain an oxidized
surface
layer overlying anoxic reduced sediment
( Hayes 1964; Fcnchcl and Ricdl 1970).
Oxygen uptake by subsurface sediment
may bc cntircly chemical ( Moore 1931))
but thin layers of surface sediment show
varying proportions of chemical and biological oxygen uptake (IIargrave 1972 and
Table 1) . Biological oxidation accounted
for an average of 30% of oxygen consumed
by salt marsh mud (Teal and Kanwisher
1961), with no clear effect of depth,
Samples of sediment and detritus held
in acrated water rapidly become dcoxygenatcd and anaerobic bacteria appear.
This is not surprising since oxygen uptake
by aquatic bacteria at 20C may range
from NO-500 ~1 02 mg-l hr-l ( Fig. 5). A
1-g sample of detritus at 20C consumes
about 1 mg 02 hr-l; thus, all of the oxygen
in 100 ml of water could bc consumed
within 1 hr. The rapid rate of oxygen consumption by bacteria in sediment may deoxygenate bottom deposits ( ZoBell 1946).
Dissolved oxygen may only penetrate the
top few millimeters of mud sediments not
exposed to water turbulence
( Hargrave
1972). Oxidative decomposition
in such
habitats must bc limited by oxygen supply.
The supply
of easily oxidized organic
592
BARRY
T,
matter must also affect rates of sediment
oxygen uptake. The higher rates of oxygen uptake by surface sediment in Lake
Esrom in November and Dcccmber may
reflect the decomposition of organic matter newly deposited after phytoplankton
blooms ( Table 1).
The stage of decomposition of detritus
is important. Organic content of fcccs may
increase or decrease with time (Newell
1965; Hargrave 1970b ) , indicating bactcrial colonization
( Fenchel 1970). Feces
were rapidly colonized (Fig. 4) and within
4 days, oxygen uptake decreased from 3.50.4 mg 02 g-l hr-l. Phragmites detritus
did not reach as high rates of oxygen uptake as feces but also showed a decrease
with time. Presumably initially high rates
result from an increase in microbial respiration as labile substrates, such as mucous
secretions are utilized.
Grazing organisms
such as protozoa, which appeared in both
feces and detritus during initial maximum
rates of oxygen uptake, would also contribute to increased oxygen consumption.
Teal (1962) observed a peak in oxygen
uptake in freshly produced Spartina dctritus during the first week of decomposition, similar to that noted with Phragmites
(Fig. 4). Explanations for differences in
the maximum rate obtained by Spartina
detritus ( 14 mg O2 g-l hr-l ) , Limnaea feccs (3.5), and Phragmites detritus ( 1.0)
during the initial period of decomposition
as well as the varied final rates of oxygen
uptake (0.25 mg O2 g-l hr-l for feces and
Phragmites, 2.0 for Spartina) may reflect
involved
the species of microorganisms
and the residual substrates.
The difficulty
of following
decomposition by only observing changes in organic
matter is illustrated
by the increase in
organic content of Phragmites during decomposition, in contrast to Spartina (Teal
1962 ) . Changes in organic content includc changes in both organic substrate
and communities of colonizing microorganisms, but changes in rates of oxygen consumption arc more easily interpreted
as
they reflect the metabolic activity of all
aerobic deorganisms associated with
HARGRAVE
composition.
The time-course of detritus
decomposition as measured by oxygen uptake seems similar for different substrates.
It is not clear why different particles of
a similar size should have even an approximately
similar rate of oxygen uptake
(Fig. 3). Decomposition processes in dctritus and mud, where the substrate is
metabolized,
may differ from those on
sand and pebbles where mineral surfaces
serve largely as a source of attachment.
If, however, only organic matter adsorbed
to surfaces is available to heterotrophic
bacteria ( ZoBell 1946)) oxygen consumption by microorganisms
associated with
sand and pcbblcs also reflects substrate
decomposition.
Oxygen uptake by mud particles tends
to be lower than might be expected on
the basis of its particle size relative to that
of detritus, and at least some of the oxygcn is used for chemical oxidation.
The
somewhat arbitrary estimate of mud particle diameter makes comparison on the
basis of particle size difficult.
Organic
matter in lake sediment ranged from 2070%; detritus always contained more than
70%. The substrates in mud may bc less
easily oxidized.
Grane Lang Lake mud
consumed the least oxygen ( 0.10 mg 02
g-l hr-l ) and also had the lowest organic
content (21.3%) of the lake sediments examined. Low annual primary production
in this lake means that its surface scdiment is older than that of the more productive
Lake Esrom or Frcderiksborg
Castle Lake (Whiteside
1970). Rybak
(1969) reported that lake sediments that
consumed less oxygen are poorer in organic matter; data summarized from other
work (see Fig. 5) shows a similar trend.
These observations
support Hayes and
MacAulay’s
( 1959) suggestion for sedimcnt oxygen uptake as an index of lake
productivity.
Particles of various types have diffcrent rates of oxygen uptake per unit surface area, but the range of values is not
large (Table 2). Estimates of surface area
per gram for various particles span four
orders of magnitude, although oxygen up-
DECOMPOSITION
OF
SEDIMENT
take per square centimeter only has a
range of two. Surface area was only measured for large pieces of detritus, and the
values assumed for other particles from
previous studies could introduce errors;
however, the cstimatcs are probably accurate enough for present calculations and
suggest some constancy in total community metabolism per unit surface for very
different types of particles.
Recolonization
experiments
Oxygen consumption
per unit weight
and the adsorption of organic matter were
both inversely related to particle size in
recolonization
experiments, but the differences were not as great as would be
expected on the basis of surface area. Oxygen uptake per unit weight and surface
area was within the range found with
freshly collected samples. All recolonized
particles had an approximaetly similar rate
of oxygen uptake on the basis of organic
content, higher than that found with the
smallest detritus particles used by Odum
and de la C*luz ( 1967). Sincc respiration
of rinsed particles was measured after
transfer to fresh nonenriched solutions, organic matter on the surfaces must have
undergone relatively rapid oxidation similar for each particle type; the organic matter and microbial populations adsorbed to
the various particles in these experiments
may also have been similar.
Recolonized particles should all have
similar rates of respiration per unit surfact if oxygen uptake by communities of
microorganisms on particle surfaces is dependent only on surface area, However,
uptake increased with increasing particle
size ( Fig. 6). There was a disproportionatcly high organic content on pcbblcs;
mud contained less organic matter than
expcctcd on the basis of its surface arca.
These differences may result from altcration of the surface characteristics of the
particles in ashing, Badcr (1962) did not
find simple adsorption
phenomena bctwecn dissolved organic compounds and
mineral particles. Various sediments differ
in adsorbing properties for different spc-
AND
DETRITUS
593
ties of bacteria (Rubcntshik et al. 1936).
ZoBell (1943) noted a logarithmic increase
extending over 18 days of bacteria attached to glass surfaces; 24 hr is probably
insufficient
for populations of colonizing
microorganisms to reach a stable level of
density and metabolism.
Bacterial
density on particle surfaces
Fenchel (1970) obscrvcd that both oxygen uptake by Thalassia detritus and the
number of bacteria, small zooflagellatcs,
and diatoms wcrc proportional to surface
arca. The number of organisms per surface area, about 3 x lo6 bacterial cells
cm-2 by direct counts, was always similar
on intact dead leaves, various sized particles, and artificial detritus after 4-6 days.
Tsernoglou and Anthony (1971) calculated
the density of bacteria by direct microscopy on freshwater sediment particles and
summarized previous estimates of bactcrial density on sand, pebbles, and soil
surfaces; depending on the source of the
sediment, there was one bacterial cell for
every 70-300 p2. If an average bacterial
ccl1 is assumed to cover 1 p2, then <I%
of the particle surface arca was colonized.
The bacterial density observed on detritus
by Fcnchel (1970) would cover about 3%
of the surface area.
Batoosingh and Anthony
( 1971) also
calculated bacterial density on pebbles dircctly by fluorescent microscopy.
Single
cells accounted for 70% of the bacterial
populations,
When colonies were present
many seemed to be chance aggregations
rather than colonies, as the individuals
were generally quite separate from each
other. An analysis of the dispersion of
the direct counts showed that the bacteria
were slightly over-dispersed on the pcbblc
surfaces. There was an average of 1 cell
/300 /.L!
These calculations
show, however approximately,
that bacterial cells do not
completely cover these sediment and detrital particles. Other habitats, such as the
surface film of stagnant water, may have
higher ccl1 densities ( Fenchel, personal
communication),
but natural
sediment
594
BARRY T. HARGRAVE
3
2
z
-2-
\\
percent
organic
\
nitrogen
‘*
‘. \
‘. ‘.
‘.
‘*.
mg O2 g-’ hr-‘x
-3 -
sand
\
-4 -I
0
‘. \
I
1
loglo
I
2
particle
(J-0
,
3
1\
4
diameter
FIG. 7.
Comparison
on logarithmic
axes of
mean particle diameter and internal surface area
of sand (from Fenchel
1969), percent organic
carbon and nitrogen
in beach sediments
(from
Longbottom
1970), bacterial plate counts in different sediments (from ZoBell 1946), and measures 0I particle oxygen consumption
taken from
Figs. 1 and 3. Solid lines are calculated regression lines presented in the respective references.
The regression for bacterial
numbers on particle
diameter is y = 4.00 - 0.94x, T = 0.95. Dotted
line indicates a slope of -1.0.
particles of various types do not appear
to bc heavily colonized. Cell counts per
unit weight give a false impression of high
numbers; the spatial distribution of microorganisms is given pcrspectivc when density is related to surface area.
Many factors are involved in the spacing
of bacterial cells. Grazing and physical
abrasion can remove cells. Algal and bacterial cells are usually found in depressions
and crevices of sand grains and pebbles
(Meadows and Anderson 1966), suggesting physical removal from raised surfaces.
Particles removed from these influences,
however, do not show an increase in bac-
tcrial numbers (Batoosingh 1964). Detritus,
more flocculant and with a higher organic
content than sand or pebbles, should offer a more suitable substrate. Still, from
Fenchel’s ( 1970) observations,
bacterial
cover in detritus is far from continuous.
Burkholder (1963) has shown that growthregulating substances are released by scdimcnt bacteria. ZoBell (1943) described a
faintly staining film which surrounds bacterial cells attached to glass slides, two
or three times the dimension of the cells
themselves, whose size increases with age.
The nature of this material is unknown.
Whatever the cause of spacing between
bacterial cells, only a fraction of the particlc surface arca is covered and the ecologically
available space is considerably
less than the total arca. Such a relationship bctwecn density and surface area
would impart some degree of similarity
to measures of community respiration per
unit area (Table 2). An upper limit to
cell density may be determined by available space, with metabolism
per cell
related to the prcscncc of oxidizable substrates, the two factors interacting to produce a relatively
constant areal rate of
community
metabolism.
This would explain why although detritus consumes more
oxygen per unit surface than do sand,
pcbblc, or mud particles, all rates vary
within narrow limits.
Longbottom
( 1970) reported that in
sediments from gently sloping, moderately
well-drained
beaches, both organic nitrogcn and carbon content varied inversely
with median particle diameter after logarithmic transformations.
The slope coefficicnts, about -1.0, and the intercept values
of the regression lines showed little scasonal change and were similar for sediments from diffcrcnt arcas. Fcnchel (1970)
has also observed an inverse linear relation (h = -1.0) bctwecn median particle
diameter and surface area of sand grains
on a logarithmic basis. These curves are
organic
redrawn in Fig. 7. Apparently
matter adsorbed or attached as microorganisms to these sediment particles is
proportional to surface arca and the rcla-
DECOMPOSITION
OF SEDIMENT
tionship is approximately similar for samples from different arcas.
The relationship
between sand grain
size and oxygen uptake per unit weight
also approaches a slope value of -1.0 (Fig.
7)) perhaps reflecting the close correlation
between sand grain diameter and surface
area; mud and detritus particles are not
spherical, so they need show no similar
relation.
Detritus oxygen consumption per unit
weight is also inversely related to particle
size but with a slope less than -1.0 (Fig.
7). The relationship bctwccn particle diameter and external surface area per gram
dry weight of Thdassia detritus too has a
slope of less than -1.0 on logarithmic axes
( Fcnchcl 1970).
Bacterial counts per unit dry weight of
sediment incrcasc with dccrcasing particle
size (ZoBell 1946), and the relationship
(b = -0.94) resembles that described for
surface area in Fig. 7. Those data were
derived from plate counts and thus only
an index of bacterial numbers is provided,
although a relatively constant proportion
of the total bacterial population may have
been measured in diffcrcnt sediment types.
For regression calculations, sand, silt, clay,
and colloidal particles have been assumed
to have diameters of 500, 50, 5, and 1 p;
these are reasonable, but arbitrary, estimates of particle size within the range
obscrvcd in the different types of scdimcnt cxamincd by ZoBell.
CONCLUSIONS
There is apparently a basically simple
relation
between surface area, organic
content, and the size and metabolism of
communities of microorganisms associated
with aquatic sediment and detritus particlcs ( Fig. 7). Undoubtedly,
tcmpcrature,
oxygen supply, and the nature of the organic substrate can modify any such relationship; variability
introduced by these
factors, howcvcr, should not detract from
the observation that particle size, and thus
the surface arca available for oxygen exchange, is an important factor in deter-
AND DETRITUS
595
mining rates of oxidation of sediment and
detrital organic matter.
The narrow range in rates of oxygen
uptake per square centimeter by different
particles of a similar size suggests that
communities of microorganisms colonizing
various surfaces may have similar rates of
metabolism. In aerobic habitats, colonization and succession may occur to the
point where all of the oxygen supply is
fully used, Measurement of oxygen uptake by communities of microorganisms
associated with sediment and detritus particlcs offers a simple method for investigating these processes.
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