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                     AREA AND ORGANIC CONTENT
                                              Bawy T. Hargrad
        Freshwater      Biological   Laboratory,   The University    of Copenhagen,    Hillergd,     Denmark

          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                               oxygen uptake by detritus,          mud, and
   Aquatic sediments and detritus consume                       sand sediments. Waksman and Hotchkiss
oxygen when stirred in aerated water, The                        ( 1938)) Teal ( 1962), and Rybak ( 1969)
oxygen uptake is an integrative measure                         suggested that oxygen uptake is related to
of all oxidative processes occurring in the                     the organic matter available for decompo-
sample, both chemical       and biological.                     sition; Odum and de la Cruz (1967) and
Reducing substances are usually rapidly                         Fenchcl (1970) d cmonstrated an invcrsc
oxidized. Respiration of the organisms as-                      relation between detritus particle size and
sociated with particles is probably pri-                        oxygen consumption.       Chemical oxidation
marily bacterial, although algae, protozoa,                     of reduced subsurface sediment may also
and fungi may also contribute.     Whatever                     be related to the concentration of reduced
populations are involved, measurements of                       substances (Gardner and Let 1965; Har-
oxygen uptake reflect the metabolism of                         grave 1972).
communities of microorganisms       involved                        Teal (1962) and Odum and de la Cruz
in the decomposition of natural substrates.                      ( 1967) found approximately      similar rates
                                                                of oxygen consumption by Spartina detri-
No measure is provided, however, of an-
                                                                tus. Thalassia decays much faster than
oxic microbial decomposition.                                   does Spartina (Wood et al. 1969)) yet oxy-
   Many workers have measured rates of                          gen uptake by detritus from these plants,
                                                                freshly collected or artificially prepared, is
    l Present address:  Fisheries Research Board of
Canada, Marinc Ecology Laboratory,       Bedford In-            similar ( Fenchel 1970). Lake Esrom scdi-
stitute of Oceanography,     Dartmouth,  Nova Scotia,           mcnts consume oxygen at rates similar to
LIMNOLOGY     AND     OCEANOGRAPHY                        583                                      JULY   1972,   v.   17( 4)
584                                    BARRY   T.   I-IARGRAVE

those observed with salt marsh mud (Har-             was used immediately.       Disks (l-cm diam)
grave 1972).                                         were cut from larger pieces of decaying
   I here compare rates of oxygen uptake             vegetation with a cork borer and lo-20
by sediment and detritus particles of dif-           mg (dry wt) were placed in bottles. In-
ferent sizes and organic content, These              cubations lasted l-2 hr in the dark at 2OC,
results, combined with previous measurc-             and bottles were rotated (4 rpm) on their
ments, show an inverse relation between              long axis to prevent oxygen depletion
particle size and oxygen consumption. The            around sedimented particles. All experi-
importance of surface area and organic               ments were carried out during summer
content is examined by calculating oxygen            and early fall when field temperatures
uptake of natural and recolonized parti-             ranged between 10 and 22C.
cles on a surface area basis. A possible                 A buffered (pH 6.8) solution of 2% For-
mechanism causing similarities and differ-           malin was used to fill some BOD bottles.
ences in rates of sediment oxygen con-               ZoBell and Brown (1944) found that a
sump tion is suggested.                              0.25% Formalin solution stopped bacterial
   I gratefully acknowledge a NATO Sci-              respiration, so oxygen consumed by parti-
ence Fellowship provided by The National             clcs in this solution was assumed to be due
Research Council of Canada, Professors E.            to chemical uptake. Additional blank bot-
Stecmann Nielsen and T. Fcnchel kindly               tles corrected for small amounts of oxygen
read the manuscript      and offered com-            uptake by the Formalin.
ments. Mr. S. Bordon calculated the re-                  Dissolved oxygen was measured by a
gression lines.                                      micro-Winkler     technique (Fox and Wing-
                                                     field 1938) with samples taken in 5-ml
         MATERIALS   AND   METI-IODS                 syringes; a solution of 1% NaN3 was added
   Sediment and detritus from freshwater             to the NaI solution to prevent interference
sources were collected from eutrophic                from reduced substances. Syringe samples
Lake Esrom and Frederiksborg          Castle         of supernatant were taken after settling
Lake, from the humic-acid brown-water                of particles. Mud particles, in particular,
Store Grib Lake, all located in northern             appear to bind the iodide liberated dur-
Zealand (Denmark) (Berg 1938), and from              ing the Winkler reaction and thus reduce
Grane Lang Lake, an oligotrophic lake in             the apparent oxygen concentration.            For-
Jutland (Whiteside 1970). Other samples              malin soIutions were titrated slowly over
were taken from Hclsing@r, Kronborg, and              10 min for accurate end-point determina-
Julebaek beaches along the northern @re-             tions. Measurements of dissolved oxygen
sund near Helsinger ( Fenchel 1969).                 were accurate to at least 0.1 mg/liter.
   Either a Kajak corer (Brinkhurst    et al.         Changes as smalI as 1% of total oxygen
1969) or a glass cylinder pushed by hand             present could be measured; changes were
into shallow sand sediment was used to               usually much greater, but concentrations
take undisturbed cores of mud and sand.              were never reduced more than 30%. Cor-
In the laboratory, samples of mud and fine           rections were made for volume displace-
                                                      mcnt throughout.
sand sediment wcrc taken from the surface
                                                         Mud and detritus were filtered onto pre-
of the cores by pipette, mixed, and drained           ashed and preweighcd         glass-fiber filters,
on filter paper. About 0.1 g wet wt was               dried ( 8OC for 24 hr ), and weighed. Sand
removed from the filter paper with a                  grains and pebbles were dried in pre-
spatula and added to 28-ml Pyrex BOD                  weighed crucibles.       Organic matter was
bottles filled by siphon with filtered aer-           determined by loss on ignition at 550C for
 ated water from the collecting area. Large           3 hr; carbonate dissociation is avoided at
pebbles, with a total weight of up to 5 g,            this temperature if ashing times are not
were added to bottles with forceps. Detri-            long (Rybak 1969). Particle size (mean
 tus collected by hand from beach margins             value of greatest dimension of randomly
                       DECOMPOSITION   OF SEDIMENT    AND DETRITUS                     585

chosen particles) of sand grains was deter-    diameter is Fenchel’s internal surface area
mined by microscopic examination; at least     divided by 16.
100 were examined when their diameter             Recolonization    expcrimcnts    were on
was less than 500 p. All pebbles greater       mud, sand, and pebbles from Lake Esrom
than l-mm diameter in the bottles were         sterilized by ashing at 550C for 3 hr. A
measured and the mean diameter dcter-          small piece of decomposing Phragmites
mined, Mud sediments consisted entirely        leaf in a solution of 1% each of glucose,
of silt and amorphous organic debris that,     peptone, and K&P04        and mud-water ex-
with gentle agitation, passed through a        tract (1 kg of wet profundal mud auto-
nylon screen with 100-p-mesh openings          claved with 1 liter of Lake Esrom water)
but clogged screens of 20 p; an average        was used for inoculum, with controls of
particle diameter of 50 p was assumed.         sterilized particles in autoclavcd lake wa-
The detritus from decaying vegetation,         tcr without detritus. After 24 hr of aera-
when not cut with a cork borer, was mea-       tion, control and inoculated particles were
sured wet on graph paper or under a            rinsed and placed in freshly filtered water,
binocular microscope.                          and oxygen uptake was measured.
    Fecal pellets were collected from three
common benthic invertebrates in Lake Es-                         RESULTS
rom. Adult Ilyoclrilus hummoniensis ( Oli-               Experimental   variables
gochaeta) and fourth instar Chironomus
anthracinus (Diptera) larvae were held in         Lake Esrom mud between 1 and 20 mg
freshly collected profundal lake mud, and      ( dry wt ) per bottle gave no significantly
fecal pellets were collected from petri        different rates of oxygen uptake per gram
dishes in which several animals had been       dry weight. Eight samples of surface sedi-
held overnight.     Limnaea palustris ( Mol-   ment taken from four profundal mud cores
lusca ) , collected with decaying Phragmi-     during June consumed 0.22 * 0.04 mg 02
tes communis, browses epiphytic material       g-l hr-l regardless of sample size. Samples
and produces abundant feces. All fecal         of sand grains (250-p diam), from a beach
pellets were kept in gently aerated lake       surface in Lake Esrom, of dry weights
water when not used within a few hours,        up to 1 g showed similar reproducibility
    Rates of oxygen consumption per unit       (220%). Two replicate samples were then
weight were compared on a surface area         used for each determination and the mean
basis by dividing rates of oxygen uptake       value recorded. Short incubations, l-2 hr,
by the number of square centimeters of         ensured sufficient oxygen yet gave mea-
sediment. Area was calculated for detritus     surable changes in concentration.        The
particles larger than 1 mm before drying       rapid oxygen uptake by some sediment
by doubling that traced on graph paper.        and detritus particles necessitated agita-
Values for mud and detritus with a par-        tion of samples. Profundal mud from Lake
ticle diameter less than 1 mm were taken       Esrom consumed 0.32 mg 02 g-l hr.-l when
from Fenchel’s (1970) estimate of total        bottles were slowly rotated and 0.08 when
surface area per gram dry weight of Tha-       standing. Oxygen uptake of beach sand
lassia detritus. Sand grain and pebble sur-    decreased by 15% when it was not stirred.
face area was estimated from a relation
between mean sand grain size and “in-                Relative importance of chemical
ternal surface” arca derived by Fenchcl                   and biological oxidation
 ( 1969), based on 10 cm3 of sample and           Oxygen uptake by sand and detritus
the assumption that sand grains were           from beaches was always completely
spherical. If the specific gravity of sand     stopped by 2% Formalin; oxygen uptake
 (quartz) is assumed to be 1.6 (Kaye and       by subsurface sediment from below 2 cm
Laby 1956), then the surface area per          in cores from Store Grib Lake and Lake
 gram dry weight for a given sand grain        Esrom was unaffected by Formalin treat-
586                                      BARRY T. HARGRAVE

TABLE 1. Effect of Formalin treatment (+ = with, - = without)     on oxygen uptake by surface (up-
per 5 mm) mud from four Danish lakes at various times of the year. All values are means of at least
                                    two separate determinations

                                                 Oxygen uptake
                              -             +     by chemical     Biological       Sediment        mg 0,
                                                    oxidation    respiration      org matter       (g org
                              (mg 0, g-1 hr-1)          (%I    (mg 0, g-1 hr-1)       (%I      matter)-1 hr-1

   15 Jun                    0.75         0.44        59             0.31           39.6            0.78
  13 Nov                     1.48         0.87        59             0.61           40.0            1.52
  15 Dee                     1.14         0.35        31             0.79           39.9            1.98
                                                                                               x    1.43
Store Grib
    5 Sep                    0.74         0.48         65            0.26           72.0           0.36
Freclcriksborg   Castle
   22 Sep                    1.34         0.73        54             0.61           45.0            1.36
Grant Lang
   15 Mar                    0.10         0.01         10            0.09            21.3           0.43

ment, indicating   that oxidative processes         of organic matter in various types of scdi-
were chemical, Surface muds (upper 5 mm             ment was standardized by expressing oxy-
as taken by pipette) from various lakes,            gen uptake on an ash-free weight basis.
however, showed varying degrees of sensi-           In sand and detritus this measure reflects
tivity to poisoning (Table 1). Oxygen was           the metabolic activity of communities of
present ( 3-5 mg/liter ) over all sampled           microorganisms      since these substrates
cores. Data from Lake Esrom show con-               showed no chemical oxidation. Mud par-
siderable seasonal variation in total oxygen        ticles did undergo chemical oxygen uptake
uptake and the amount susceptible to For-           and this has been subtracted in the calcu-
malin poisoning.                                    lations of biological respiration in Table
                                                     1. The range of values of oxygen uptake
      Particle size and organic content             by various particles was reduced by these
   Oxygen uptake by sand grains, detritus           calculations, and the effect of particle size
particles, and mud sediments was differ-            was enhanced (Fig. 3). Oxygen uptake by
ent per unit weight and each varied on the          all material fell within the range [O.l-10.0
basis of mean particle diameter (Fig. 1).           mg 02 (g org matter)-l hr-l] observed for
With the logarithmic      transformation    of      detritus ( Fig. 1) largely because values
both axes, Fig. 1 reveals a linear, inverse         for oxygen uptake by sand grain commu-
relation between particle diameter and ox-          nities, when expressed on an ash-free ba-
ygen uptake. Values for mud were omitted            sis, were raised. Although differences are
from the regression calculations because of         large, organic matter in various muds was
the inaccurate estimation of particle size.         oxidized at much lower rates than detritus
   Oxygen uptake for a given particle diam-         particles of similar size.
eter was two to three orders of magnitude
higher for detritus than for sand. Sand                          Stage of decomposition
grains and pebbles contained less than 1%              Fresh snail fecal pellets (about 0.5-mm
organic matter while mud and detritus               diam and 2 mm long) contained 80-90%
particles contained 40-90% organic matter.          organic matter. This always increased as
After logarithmic transformations,     oxygen       they aged, probably from organic matter
uptake was linearly related to organic con-         removed from solution by microorganisms
tent (Fig. 2).                                      colonizing their surfaces, although it could
   The effect of differences in percentage          also result from leaching of inorganic salts.
                                  DECOhXTi’OSITION        OF     SEDIMENT   AND   DETRITUS                                            587


                                                sand                                              ,

                                                           . x
        -4 -I 0 8c,““I   1 8 I II”11 1 18““‘I   ’ “A?
           0           1           2          3           4
                     loglo   particle         diameter
    FIG. 1. Relation between mean particle diam-
eter and oxygen uptake per gram dry weight of                            FIG. 2. Relation between percent organic mat-
sand, mud, and detritus              from various         aquatic    ter and oxygen uptake per gram dry weight of
habitats.                                                            different  particles described in Fig. 1. Regression
    Solid circle-detritus       from Lake Esrom shore                line, calculated    omitting bacteria and mud sam-
 (1, mean value for five species of deciduous tree                   ples, y = -2.15 + 0.90x (r = 0.91, sE of slope
leaves; 2, unidentified       reed detritus; 3, Phrugmi-             0.075, significant   at P = 0.05).
tes leaves); solid triangle-invertebrate               feces (l-
day-old ) ( 1, Limnaea            palustris;      2, Ilyodrilus
hammoniensis.       3, Chironomus          anthrucinus);     solid   days the rate of oxygen uptake declined
square-sand       and unknown seaweed detritus from
Julebaek beach; cross-sand,               detritus,   and mud
                                                                     to 0.55 mg O2 g-1 hr-l, followed by a
from Store Grib Lake; open triangle-Frederiks-                       slow decrease to 0.25 after holding for 20
borg Castle lake mud; point-Grane                   Lang Lake        days. The decline in oxygen uptake was
profundal     mud; circled         cross-IIelsinggr         beach    accompanied by successions of communi-
sand; circled       point-Kronborg             beach     pebbles;
open square-sediment              bacteria       (Pseudomonas
                                                                     ties of microorganisms associated with the
spp.) cultured from Lake Esrom surface profundal                     fecal material. Ciliates, abundant after the
mud; open circles-Fenchel               (1970), Thalassia de-        first day, declined after the fifth. Fungal
tritus;   squared points-Odum               and de la Cruz           hyphac grew rapidly       and changed the
 ( 1967), Spartina detritus.                                         pellets from brown to white within 12 hr.
    Regression lines-detritus:            y = 1.45 - 0.52 x ( r
 = 0.65, SE of slope 0.17); sand: y = -0.20 - 0.85                       Phragmites leaves, collected dry from
x (r= 0.95, SE of slope 0.07). Slopes are signifi-                   dead plants in November, were placed in
 cantly different     from zero (P = 0.05).             Data for     aerated lake water in the laboratory, Disks
mud, bacteria, Thalassia detritus ( Fenchel 1970))
 and Spartina detritus (Odum and de la Cruz 1967)
                                                                     of leaf material tested immediately     con-
not included in regression calculations.                             tained 82.5% organic matter and consumed
                                                                     0.22 mg 02 g-l hr-l (Fig. 4). After 3 days
Oxygen uptake by microorganisms on fe-                               oxygen uptake had increased to 1.0 mg
cal pellets used within 6 hr of production                           02 g-l hr-l and leaf material contained
was three times faster than when pellets                             90% organic matter. During the next 2
were first held for 12 hr (Fig, 4). After 3                          days there was little change in organic
588                                         BARRY T. HARGRAVE

                                                                                      c      0 fecal   pellets

                                                                                     “,~~~~~‘, Phragmites        detritus


                                                                       0        10          20         30          40
                    log ,O particle    diameter                                      Time    (days)
                                                             FIG. 4. Changes in oxygen uptake by Limnuea
   FIG. 3. Relation between mean particle diam-           feces and Phragmites detritus held at 20C in aer-
eter and oxygen uptake per gram organic matter            ated Lake Esrom water. Samples removed for use
(calculated  from Figs. 1 and 2 ). Symbols as in          in short-term   experiments  at various times. a-
Fig. 1. Regression line, calculated omitting mud,         Detritus prepared from plant leaves collected dry;
bacteria, and data (line joining points) from Odum        b-detritus    wet and partly     decomposed   when
and de la Cruz (1967), y = 2.07 -0.69x       (r = 0.79,   collected.
SE of slope 0.10, significant   at P = 0.05).

                                                                           Previous measurements
content ( 90.5% ) , but oxygen consumption                    Odum and de la Cruz (1967) and
fell to the original level. Oxygen uptake                 Fenchel ( 1970) related oxygen uptake to
remained constant over the following       34             particle size of Spartina and ThaZussiu de-
days,    while organic matter slowly in-                  tritus. Their results, plotted in Fig, 1, are
creased to 98.5%.                                         of the same magnitude as mine for detri-
    In a similar experiment with Phragmites               tus from different sources.
                                                              I have used organic contents of sedi-
leaves collected as wet detritus from be-
                                                          ment and detrital material reported by
side Lake Esrom, oxygen uptake, initially
                                                          various workers as a basis for comparing
0.5 mg 02 g-l hr-l, decreased steadily,                   rates of oxygen uptake per unit dry weight
while organic matter increased from 94.3-                 (Fig. 5); sewage particles, artificial stream
98.0%. The final constant rate of oxygen                  periphyton,   aquatic vascular plants, and
consumption by this material was similar                  aquatic bacteria are included for compari-
to those by freshly wetted leaves and                     son. When expressed on logarithmic axes,
Limnaea feces at the end of the holding                   these data show the same trend and span
period (Fig. 4). This value (0.25 mg 02                   the same range as those from this study
g-1 hrl)     falls within the range observed               (Fig. 2). Odum and de la Cruz ( 1967)
for detrital material from other sources                  measured both organic content and parti-
 (Fig. 1).                                                cle size of decomposing Spartina detritus.
                                    DECOMXPOSITION            OF SEDIUENT         AND DETRITUS                                    589

                                                                                          m     mg O2 g-’ hr-’
                                                                                          0     percent   organic    matter
                                                                                          m     mg O2 (g organic      matter )-’ hr-’
                                                                                          m     mg o2 x10-~ cm-* hr-’


                                                                                              particle    diameter     CJI)
                                                                                          mud             sand         pebbles

                                                                           FIG. 6. Mean oxygen consumption         and organic
                         log,o     percent       organic                content of triplicate    samples of ashed mud, sand,
                                    matter                              and pebbles from Lake Esrom after 24 hr of
   FIG. 5. Comparison             of organic content and ox-            exposure to Phragmites       detritus in a nutrient-cn-
ygen uptake per gram dry weight for different                           riched solution.     Control samples, not exposed to
types of sediment and detritus, aquatic vascular                        detritus and nutrients,      contained  no mensurable
plants, periphyton        communities,       and bacterial cells        organic matter and consumed no oxygen.
from previous         studies.      Circles indicate        average
values for measurements at about 20C. Lines rep-
resent range of published observations.                                 Oxygen uptake, on an ash-free basis, fol-
    l-Johnson         ( 1936 ) , resting      marine bacteria;          lows the trend of my data and falls within
2-ZoBell        and Stadler (1940),            multiplying       lake   the same order of magnitude when com-
bacteria; 3-Liagino            and Kusnetzov        (cited in Zo-
Bell and Stadler 1940), lake bacteria;                     4-Har-
                                                                        pared with particle size ( Fig. 3).
grave (1969),         estimated value for lake sediment
bacteria; 5-Gessner            ( 1959), various aquatic vas-                         Particle surface area
cular     plants;     6-McIntire          ( 1966))      periphyton         All particles considered in this study
communities        in artificial    streams; 7-Teal          (1962),
Spartina detritus during 4-week decay period; 8-                        consumed between 0.01 and 1.0 x 1O-3 mg
Odum and de la Cruz ( 1967), Spartina detritus;                         02 cm-2 hr-l with the exception of freshly
9-Fenchel         ( 1970), Thalassia detritus.                          produced Limnaea feces (Table 2); oxygen
    N-Water          Pollution      Research Rep. ( 1968),
                                                                        consumption of fcccs fell to within the
suspended solids in treated sewage effluent;                   ll-
DiSalvo ( 1971), coral reef regenerative                 sediment;      range observed for all other particles
12-I&rnerblad           (1930), mean value for 14 Swed-                 within   3 days. Dctri tus particles con-
ish lakes ( assumed 2 g dry wt/flask);                         13-      sumed more oxygen on an arcal basis than
Miyadi      (cited in ZoBell 1946), lake sediments;
14-Waksman           and Hotchkiss (1938), marine sedi-                 pebbles, sand, or mud. There was no con-
ments from Woods Hole; 15-Kato                       ( 1956), ma-
rine bottom sediments from the northern                       Japan
Sea; 16-Teal         and Kanwisher (1961), surface salt-
marsh mud; 17-Gardner                 and Let ( 1965), Lake             (1969),   black   clots, Polish lakes of varying       trophic
Mendota sediment (initial 3-day rate); 18-Rybak                         type.
590                                                     BARRY T. IIARGRAVE

TADLE 2.     Comparison of mean particle diameter                   recolonized pebbles, however, was an or-
(p), estimated surface area per gram dry weight
                                                                    der of magnitude higher than that of
(A), and oxygen uptake per unit surface area (C)
for various types of particles.  Data fur oxygen                    freshly collected material. There were few
         uptake per gram (B) from Fig. 1                            protozoa in the detritus used for inocula-
                                                                    tion and thus oxygen consumption prob-
      and source                           A        B        C
                                                                    ably reflects only bacterial respiration.
                                                                        No organic matter remained on particles
Pebbles                                                             after ashing, but after 24 hr of exposure
  Kronborg         beach        9,000     1.2 0.00012       0.10    to the nutrient solution and detritus par-
                                7,800     1.5 0.00030       0.20
                                                                    ticles a loss on ignition was measured in
                                5,340     1.9 0.00655       0.2.9
                                4,000     2.7 O.OC@70       0.26    all samples (Fig. 6). The percentage or-
  Esrom      beach              1,914     5.6 0.0012        0.21    ganic matter was inversely related to par-
                                1,260     6.5 0.0011        0.17    ticle size but all particles contained an
Sand                                                                order of magnitude less organic matter
  Esrom      beach               550     21.9    0.0058     0.26    than naturally occurring samples of simi-
                                 3G6     31.2    0.0028     0.09    lar type.
  Helsing@r        beach         350     32.0    0.0046     0.14        Oxygen uptake per gram organic matter,
                                 185     62.,5   0.0064     0.10    which ranged from 9-28, was not related
  Julebmk      beach             248     50.0    0.0086     0.17
                                                                    to particle diameter (Fig, 6). Oxygen
Lake mud                                                            consumption     per unit surface area in-
  Esrom                            50   6,000    0.86       0.14    creased with increasing particle size; the
   Store Crib                      50   6,000    0.74       0.12    range of values was within that observed
   Grane Lang                      50   6,000    0.10       0.02
   Frederiksborg       Castle      50   6,000    1.34       0.22
                                                                    with natural particles (Table 2).
Detritus                                                                             DISCUSSION
  Esrom shore debris      -     -  0.33                     0.30
  Wet elm leaves          -     -  0.18                     0.42
                                                                        The enumeration of microorganisms can-
  Phragmites              -     -  0.24                     0.42    not serve as a measure of their importance
  E quisetum              -     -  0.10                     0.26    in proccsscs of decomposition.     There may
  Limnaea feces, fresh 5001 650 3.50                        5.38    be no clcarcut relation between numbers
       3-day-old         500   650 0.55                     0.85    and metabolic rate. The dynamic nature
  Spartina               239 1,050 0.63                     0.60
   (Odum and de          150 1,800 1.62                     0.90    of microbial populations also makes esti-
    la Cruz 1967 )        64 4,200 1.81                     0.43    mates of population size of limited use;
  Thalassia            1,000   420 0.40                     0.95    grazing may stimulate or retard cell divi-
  (Fcnchel       1970)   400   850 0.60                     0.71    sion and substrate changes determined by
                                  100 2,500 1.05            0.42
                                                                    species succession may continuously affect
                                                                    population    size. These limitations   prob-
                                                                    ably account for the lack of correlation
sistent relation between oxygen uptake per                          between sediment organic content and
square centimeter and particle size.                                indices ( plate counts) of bacterial biomass
                                                                     (Cooper et al. 1953; Volkmann and Oppen-
             Recolonization           experiments                   heimer 1962; Anthony and Hayes 1964).
   Previously   ashed pebbles, sand, and                            Also, the amount of total organic matter
mud, held in sterilized water for 24 hr,                            in sediment does not indicate its availa-
showed no measurable oxygen consump-                                bility to cithcr microorganisms ( Waksman
tion. After 24 hr of exposure to Phragrni-                           and Hotchkiss 1938) or invcrtcbratcs (Har-
tes detritus in an enriched medium, rinsed                           grave 1970a).
samples of mud and sand consumed oxy-                                   Measurement     of oxygen consumption
gen at rates inversely related to particle                           appears to be a more useful basis for com-
size and in the range of similarly sized                             paring microbial activity in different types
particles with natural communities of mi-                            of sediment and detrital material. Hayes
croorganisms (Fig. 6). Oxygen uptake by                              and MacAulay (1959) suggest that oxygen
                         DECOMPOSITION   OF   SEDIMENT   AND   DETRITUS                     591

uptake by mixed mud may represent an             minerals (Gardner and Lee 1965) and
integrative measure of lake productivity.        slow microbial oxidation of organic matc-
Although they measured oxygen consumed           rial such as lignin and humic complexes.
by restratified mud-water   systems, there       Whatever the cause of the time-dependent
was a linear relation between oxygen up-          decrease in oxygen uptake, short-term ex-
take and “lake quality index,” a value           pcrimcnts give maximum rates of oxygen
derived from an estimate of fish yield.          consumption, which might reflect rates oc-
                                                 curring in nature if samples were taken
          Experimental    variables              from well-aerated areas.
   The interpretation      of oxygen uptake          The depth from which a sample is taken
necessitates standardization of those exper-     can be important. The variable proportion
imcntal variables which might affect mea-        of chemical oxidation in lake muds (Lon-
sured rates. For example, Waksman and            ncrblad 1930 and Table 1) differs from
Hotchkiss (1938) found shaking to have           marinc sand sediment where sterilization
no effect, but total oxygen uptake de-           completely stopped oxygen uptake (Waks-
creased with the amount of sediment per          man and Hotchkiss 1938). The absence
bottle; I observed opposite effects of shak-     of chemical oxidation of beach sand and
ing and sample size. They left sediment           detritus probably results from the well-
standing for up to 30 days, stirring it by       oxygenated     conditions  on wave-washed
hand several times daily.       In long-term     beaches where few reducing substances
experiments, oxygen dcplction around set-         exist ( Fenchel 1969). Usually, however,
tled particles would lower the rate of oxy-      sediments contain an oxidized           surface
gen uptake. The effect would be greater          layer overlying anoxic reduced sediment
with larger samples ( Kato 1956). Oxygen          ( Hayes 1964; Fcnchcl and Ricdl 1970).
uptake by mud sediments, because of the           Oxygen uptake by subsurface sediment
small particle size and often high propor-       may bc cntircly chemical ( Moore 1931))
tion of chemical oxidation ( Table I), may       but thin layers of surface sediment show
bc more affected by agitation and size of        varying proportions of chemical and bio-
sample than sand sediments. The small            logical oxygen uptake (IIargrave 1972 and
range of weights used hcrc (1-28 mg dry          Table 1) . Biological oxidation accounted
wt/28 ml) may not have been sufficient           for an average of 30% of oxygen consumed
to show such an effect.                          by salt marsh mud (Teal and Kanwisher
                                                  1961), with no clear effect of depth,
              Sample variability                     Samples of sediment and detritus held
   Changes in rates of oxygen consumption        in acrated water rapidly become dcoxy-
by sediment and detritus with time can           genatcd and anaerobic bacteria appear.
be expected as easily oxidized substances        This is not surprising since oxygen uptake
disappear. Previous studies with various         by aquatic bacteria at 20C may range
types of scdimcnt (Anderson 1939; Kato           from NO-500 ~1 02 mg-l hr-l ( Fig. 5). A
1956; Teal and Kanwisher 1961; Gardner           1-g sample of detritus at 20C consumes
and Lee 1965; Hamilton and Greenfield            about 1 mg 02 hr-l; thus, all of the oxygen
1967; Rybak 1969; Fenchel 1969; DiSalvo          in 100 ml of water could bc consumed
1971) all show a time-dependent decrease         within 1 hr. The rapid rate of oxygen con-
in oxygen consumption although the time          sumption by bacteria in sediment may de-
scale is different.  The immcdiatc effect        oxygenate bottom deposits ( ZoBell 1946).
may represent oxygen uptake by reduced           Dissolved oxygen may only penetrate the
minerals, such as ferrous iron and ferrous       top few millimeters of mud sediments not
carbonate, and microbial decomposition of        exposed to water turbulence        ( Hargrave
easily oxidized organic substances. Long-        1972). Oxidative decomposition        in such
term slow rates of oxygen consumption            habitats must bc limited by oxygen supply.
may bc due to acid-insoluble iron sulfide            The supply   of easily oxidized organic
592                                    BARRY   T,    HARGRAVE

matter must also affect rates of sediment             composition.        The time-course of detritus
oxygen uptake. The higher rates of oxy-               decomposition as measured by oxygen up-
gen uptake by surface sediment in Lake                take seems similar for different substrates.
Esrom in November and Dcccmber may                        It is not clear why different particles of
reflect the decomposition of organic mat-             a similar size should have even an approx-
ter newly deposited after phytoplankton               imately      similar rate of oxygen uptake
blooms ( Table 1).                                     (Fig. 3). Decomposition processes in dc-
    The stage of decomposition of detritus            tritus and mud, where the substrate is
is important. Organic content of fcccs may            metabolized,        may differ from those on
increase or decrease with time (Newell                sand and pebbles where mineral surfaces
1965; Hargrave 1970b ) , indicating bactc-            serve largely as a source of attachment.
rial colonization    ( Fenchel 1970). Feces           If, however, only organic matter adsorbed
were rapidly colonized (Fig. 4) and within            to surfaces is available to heterotrophic
4 days, oxygen uptake decreased from 3.5-             bacteria ( ZoBell 1946)) oxygen consump-
0.4 mg 02 g-l hr-l. Phragmites detritus               tion by microorganisms           associated with
did not reach as high rates of oxygen up-             sand and pcbblcs also reflects substrate
take as feces but also showed a decrease              decomposition.
with time. Presumably initially high rates                Oxygen uptake by mud particles tends
result from an increase in microbial respi-           to be lower than might be expected on
ration as labile substrates, such as mucous           the basis of its particle size relative to that
secretions are utilized.     Grazing organisms        of detritus, and at least some of the oxy-
such as protozoa, which appeared in both              gcn is used for chemical oxidation.           The
feces and detritus during initial maximum             somewhat arbitrary estimate of mud par-
rates of oxygen uptake, would also con-               ticle diameter makes comparison on the
tribute to increased oxygen consumption.              basis of particle size difficult.         Organic
    Teal (1962) observed a peak in oxygen             matter in lake sediment ranged from 20-
uptake in freshly produced Spartina dctri-            70%; detritus always contained more than
tus during the first week of decomposi-               70%. The substrates in mud may bc less
tion, similar to that noted with Phragmites           easily oxidized.        Grane Lang Lake mud
 (Fig. 4). Explanations for differences in            consumed the least oxygen ( 0.10 mg 02
the maximum rate obtained by Spartina                 g-l hr-l ) and also had the lowest organic
detritus ( 14 mg O2 g-l hr-l ) , Limnaea fe-          content (21.3%) of the lake sediments ex-
ccs (3.5), and Phragmites detritus ( 1.0)             amined. Low annual primary production
during the initial period of decomposition            in this lake means that its surface scdi-
as well as the varied final rates of oxygen           ment is older than that of the more pro-
uptake (0.25 mg O2 g-l hr-l for feces and             ductive       Lake Esrom or Frcderiksborg
Phragmites, 2.0 for Spartina) may reflect              Castle Lake (Whiteside           1970). Rybak
the species of microorganisms           involved       (1969) reported that lake sediments that
 and the residual substrates.                          consumed less oxygen are poorer in or-
    The difficulty   of following    decomposi-        ganic matter; data summarized from other
tion by only observing changes in organic             work (see Fig. 5) shows a similar trend.
matter is illustrated     by the increase in           These observations         support Hayes and
 organic content of Phragmites during de-              MacAulay’s        ( 1959) suggestion for sedi-
 composition, in contrast to Spartina (Teal            mcnt oxygen uptake as an index of lake
 1962 ) . Changes in organic content in-               productivity.
 cludc changes in both organic substrate                   Particles of various types have diffcr-
 and communities of colonizing microorga-              ent rates of oxygen uptake per unit sur-
 nisms, but changes in rates of oxygen con-            face area, but the range of values is not
 sumption arc more easily interpreted           as     large (Table 2). Estimates of surface area
 they reflect the metabolic activity of all            per gram for various particles span four
 organisms associated with          aerobic de-        orders of magnitude, although oxygen up-
                         DECOMPOSITION   OF   SEDIMENT       AND     DETRITUS                        593

take per square centimeter only has a             ties of bacteria (Rubcntshik et al. 1936).
range of two. Surface area was only mea-          ZoBell (1943) noted a logarithmic increase
sured for large pieces of detritus, and the       extending over 18 days of bacteria at-
values assumed for other particles from           tached to glass surfaces; 24 hr is probably
previous studies could introduce errors;          insufficient for populations of colonizing
however, the cstimatcs are probably accu-         microorganisms to reach a stable level of
rate enough for present calculations and          density and metabolism.
suggest some constancy in total commu-
nity metabolism per unit surface for very                Bacterial    density on particle surfaces
different types of particles.                         Fenchel (1970) obscrvcd that both oxy-
                                                  gen uptake by Thalassia detritus and the
        Recolonization   experiments              number of bacteria, small zooflagellatcs,
   Oxygen consumption        per unit weight      and diatoms wcrc proportional to surface
and the adsorption of organic matter were         arca. The number of organisms per sur-
both inversely related to particle size in        face area, about 3 x lo6 bacterial cells
recolonization    experiments, but the dif-       cm-2 by direct counts, was always similar
ferences were not as great as would be            on intact dead leaves, various sized parti-
expected on the basis of surface area. Ox-        cles, and artificial detritus after 4-6 days.
ygen uptake per unit weight and surface           Tsernoglou and Anthony (1971) calculated
area was within the range found with              the density of bacteria by direct micros-
freshly collected samples. All recolonized        copy on freshwater sediment particles and
particles had an approximaetly similar rate       summarized previous estimates of bactc-
of oxygen uptake on the basis of organic          rial density on sand, pebbles, and soil
content, higher than that found with the          surfaces; depending on the source of the
smallest detritus particles used by Odum          sediment, there was one bacterial cell for
and de la C*   luz ( 1967). Sincc respiration     every 70-300 p2. If an average bacterial
of rinsed particles was measured after            ccl1 is assumed to cover 1 p2, then <I%
transfer to fresh nonenriched solutions, or-      of the particle surface arca was colonized.
ganic matter on the surfaces must have            The bacterial density observed on detritus
undergone relatively rapid oxidation simi-        by Fcnchel (1970) would cover about 3%
lar for each particle type; the organic mat-      of the surface area.
ter and microbial populations adsorbed to             Batoosingh and Anthony        ( 1971) also
the various particles in these experiments        calculated bacterial density on pebbles di-
may also have been similar.                       rcctly by fluorescent microscopy.        Single
   Recolonized particles should all have          cells accounted for 70% of the bacterial
similar rates of respiration per unit sur-        populations,     When colonies were present
fact if oxygen uptake by communities of           many seemed to be chance aggregations
microorganisms on particle surfaces is de-        rather than colonies, as the individuals
pendent only on surface area, However,            were generally quite separate from each
uptake increased with increasing particle         other. An analysis of the dispersion of
size ( Fig. 6). There was a disproportion-        the direct counts showed that the bacteria
atcly high organic content on pcbblcs;            were slightly over-dispersed on the pcbblc
mud contained less organic matter than            surfaces. There was an average of 1 cell
expcctcd on the basis of its surface arca.        /300 /.L!
These differences may result from altcra-             These calculations    show, however ap-
tion of the surface characteristics of the        proximately,     that bacterial cells do not
particles in ashing, Badcr (1962) did not         completely cover these sediment and de-
find simple adsorption        phenomena bc-       trital particles. Other habitats, such as the
twecn dissolved organic compounds and             surface film of stagnant water, may have
mineral particles. Various sediments differ       higher ccl1 densities ( Fenchel, personal
in adsorbing properties for different spc-        communication),       but natural     sediment
594                                                                BARRY T. HARGRAVE

                                                                                    tcrial numbers (Batoosingh 1964). Detritus,
                                                                                     more flocculant and with a higher organic
                                                                                     content than sand or pebbles, should of-
                                                                                    fer a more suitable substrate. Still, from
                                                                                    Fenchel’s ( 1970) observations,        bacterial
       2                                                                            cover in detritus is far from continuous.
                                                                                    Burkholder (1963) has shown that growth-
                                                                                    regulating substances are released by scdi-
                                                                                    mcnt bacteria. ZoBell (1943) described a
                                                                                    faintly staining film which surrounds bac-
                                                                                    terial 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
                 percent                         ‘. \
                  organic                               ‘*                          bacterial cells, only a fraction of the par-
      -2-                 \                               ‘. \
                     nitrogen                                    ‘. ‘.              ticlc surface arca is covered and the eco-
                                                                         ‘.         logically   available space is considerably
      -3 -                                  mg O2 g-’ hr-‘x                         less than the total arca. Such a relation-
                                                                                    ship bctwecn density and surface area
                                  \                                                 would impart some degree of similarity
      -4 -I       I         I           ,                 1\                        to measures of community respiration per
         0        1         2           3                4
                                                                                    unit area (Table 2). An upper limit to
              loglo    particle       diameter
                                                                                    cell density may be determined by avail-
                                                                                    able space, with metabolism           per cell
    FIG. 7.   Comparison     on logarithmic     axes of                             related to the prcscncc of oxidizable sub-
mean particle diameter and internal surface area
                                                                                    strates, the two factors interacting to pro-
of sand (from Fenchel         1969), percent organic
carbon and nitrogen      in beach sediments       (from                             duce a relatively       constant areal rate of
Longbottom     1970), bacterial plate counts in dif-                                community      metabolism.     This would ex-
ferent sediments (from ZoBell 1946), and mea-                                       plain why although detritus consumes more
sures 0I particle oxygen consumption        taken from                              oxygen per unit surface than do sand,
Figs. 1 and 3. Solid lines are calculated regres-
sion lines presented in the respective references.
                                                                                    pcbblc, or mud particles, all rates vary
The regression for bacterial     numbers on particle                                within narrow limits.
diameter is y = 4.00 - 0.94x, T = 0.95. Dotted                                          Longbottom      ( 1970) reported that in
line indicates a slope of -1.0.                                                     sediments from gently sloping, moderately
                                                                                    well-drained    beaches, both organic nitro-
particles of various types do not appear                                            gcn and carbon content varied inversely
to bc heavily colonized. Cell counts per                                            with median particle diameter after loga-
unit weight give a false impression of high                                         rithmic transformations.      The slope coeffi-
numbers; the spatial distribution of micro-                                         cicnts, about -1.0, and the intercept values
organisms is given pcrspectivc when den-                                            of the regression lines showed little sca-
sity is related to surface area.                                                    sonal change and were similar for sedi-
   Many factors are involved in the spacing                                         ments from diffcrcnt arcas. Fcnchel (1970)
of bacterial cells. Grazing and physical                                            has also observed an inverse linear rela-
abrasion can remove cells. Algal and bac-                                           tion (h = -1.0) bctwecn median particle
terial cells are usually found in depressions                                       diameter and surface area of sand grains
and crevices of sand grains and pebbles                                             on a logarithmic basis. These curves are
 (Meadows and Anderson 1966), suggest-                                              redrawn in Fig. 7. Apparently           organic
ing physical removal from raised surfaces.                                          matter adsorbed or attached as micro-
Particles removed from these influences,                                            organisms to these sediment particles is
however, do not show an increase in bac-                                            proportional to surface arca and the rcla-
                        DECOMPOSITION    OF SEDIMENT       AND DETRITUS                                   595

tionship is approximately similar for sam-       mining rates of oxidation of sediment and
ples from different arcas.                       detrital organic matter.
    The relationship   between sand grain            The narrow range in rates of oxygen
size and oxygen uptake per unit weight           uptake per square centimeter by different
also approaches a slope value of -1.0 (Fig.      particles of a similar size suggests that
7)) perhaps reflecting the close correlation     communities of microorganisms colonizing
between sand grain diameter and surface          various surfaces may have similar rates of
area; mud and detritus particles are not         metabolism. In aerobic habitats, coloniza-
spherical, so they need show no similar          tion and succession may occur to the
relation.                                        point where all of the oxygen supply is
    Detritus oxygen consumption per unit         fully used, Measurement of oxygen up-
weight is also inversely related to particle     take by communities of microorganisms
size but with a slope less than -1.0 (Fig.       associated with sediment and detritus par-
7). The relationship bctwccn particle di-        ticlcs offers a simple method for investi-
ameter and external surface area per gram        gating these processes.
dry weight of Thdassia detritus too has a
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