SIZE CLASSES OF ORGANIC
CARBON
IN SEAWATER
Jonathan H. Sharp1
Department
of Oceanography,
Dalhousic
University,
Halifax,
Nova Scotia
ABSTRACT
Using carbon analyses, four size classes of organic matter in seawater are investigated.
An appreciable portion of the organic matter is smaller than the usually defined particulate
class, but is most probably not truly dissolved.
This portion can be segrcgatcd usinlg very
fine membrane filters and using membranes for forced dialysis.
It is suggested that this
“subparticulate”
class should be considered as colloidal organic matter.
Membrane-mat filters have been used in
oceanographic research since 1952 (Goldberg et al. 1952); both these and microporous sheet filters arc now widely used
to separate “particulate”
and “dissolved”
matter. These classes, also referred to as
suspended and soluble, have been arbitrarily delineated according to the nature
of the filters used rather than by strict physical definitions.
This is convenient for analytical purposes, but it is misleading to
consider these classes as actually being
particulate and dissolved.
A dissolved organic molecule in an aqueous medium is one in which minimum free
energy is attained by hydration of all potentially hydrophilic sites on the molecule.
Any association of molecules allowing for
loss of water of hydration and formation
of a less hydrophilic
species tends to remove the resulting molecular-associate from
solution. A clear barrier between dissolved
and particulate matter would be a difficult
thing to describe, especially in a complex
ionic solution like seawater. I-Iowever, organic matter in the colloidal size range
should not be considered as dissolved. By
definition, colloidal particles are those between about 1 pm and 1 nm in their smallest dimensions (Vold and Vold 1966). An
attempt is made here to examine colloidal
organic carbon in seawater as well as “particulate” and total organic carbon,
This paper is based on a portion of a
dissertation submitted to Dalhousie Uni’ Present address: Institute of Marine Resources,
Scripps Institution
of Oceanography,
P. 0. Box
109, La Jolla, California 92037.
LIMNOLOGY
AND
OCEANOGRAPHY
versity. For aid and advice in this work, I
am especially indebted to G. A. Riley and
I thank both of them,
I?. J. Wangcrsky.
J. R. Beers, P. M. Williams,
0. HolmIIansen, and G. E. Dawson for helpful
criticism of the manuscript.
METHODS
For the remainder of this paper, the
terms “particulate” and “dissolved” are used
conventionally;
that is, particulate is the
matter retained by and dissolved is the
matter passing through a membrane filter.
Two different membrane filters were used
for the work described, and it is recognized that the stated pore sizes of these
filters are not accurate when they are used
with seawater (Sheldon and Sutcliffe 1969;
Sheldon 1972). Although Sheldon and Sutcliffe found discrepancies in average pore
sizes, this inaccuracy is not important here
since the differences in pore sizes used in
my experiment were very great.
Four classes of organic matter in seawater samples were assessed: total, particulate, colloidal class 1, and colloidal class
2. The particulate class included all particles retained by a 0.8-pm pore size membrane filter. The first colloidal class was
calculated by subtracting the value of a
0.025-pm pore size filtrate from that of the
unfiltered sample. A second colloidal class
was calculated by subtracting the value of
a 0.003-pm pore size filtrate from that of
the unfiltered sample. Total organic carbon was determined on the unfiltered samplc. Hence, both colloidal classes included
the particulate fraction and the second col-
441
MAY
1973,
V. 18(3)
442
JONATHAN
Table 1. Organic carbon data from the
cruise. Station number and depth (in m)
in sample column. Particulate
and total
in mg C liter-‘. Particulate values dividecl
values times 100 are listed in percent
Sackville
are listed
data are
by total
column
Sample
Particulate
Total
Percent
12-50
-75
-100
-1500
-2000
-2500
13-5
-25
-50
0.028
0.015
0.016
0.008
0.005
0.025
0.061
0.049
0.041
0.023
0.011
0.009
0.005
0.004
0.006
0.004
0.047
0.080
0.010
0.005
0.006
0.016
0.002
0.004
0.004
0.011
1.25
1.18
1.23
1.07
1.18
1.14
1.50
1.13
2.23
1.30
1.27
0.77
0.41
2.15
0.010
0.009
0.006
0.004
0.005
0.012
0.003
0.003
0.003
0.002
0.045
0.024
0.007
0.003
0.003
0.003
0.002
0.004
0,005
0.004
1.53
1.54
1.35
1.53
1.39
1.34
1.43
1.39
1.52
1.42
1.49
1.38
1.22
1.16
1.08
1.14
1.07
1.00
1.24
1.07
-100
-500
-1000
-2000
-3000
-4000
-4500
14-10
-50
-500
-1000
-1500
-2000
-2500
-3000
-3450
-3950
15-200
-300
-400
-500
-600
-1000
-1500
-1600
-1700
-1800
16-10
-50
-100
-500
-1000
-1200
-1400
-1600
-1800
-2000
1.27
0.83
0.91
0.94
0.80
0.84
1.03
1.09
1.30
1.16
1.04
0.83
0.86
0.91
0.76
0.95
0.96
0.77
4.04
4.36
3.23
2.78
1.25
0.96
0.61
0.45
0.60
0.32
3.48
6.87
0.94
0.57
0.68
1.71
0.31
0.38
0.38
1.47
0.63
0.58
0.48
0.26
0.38
0.92
0.18
0.24
0.18
0.14
3.01
1.76
0.61
0.28
0.26
0.25
0.17
0.39
0.39
0.33
loidal class also included the first colloidal
class.
Samples were collected in the western
central North Atlantic Ocean during cruises
on the CSS Damon and CFAV Sackville;
station positions are listed elsewhere ( Sharp
1973). Particulate organic carbon was determined by combustion at high temper-
I-1. SHARP
Table
2.
Particulate
organic
carbon
as a percent
marine envi2this
work; 31971; b-sharp
of total organic carbon for various
ronments.
(l-Gordon
F&on
et al. 1967;
1971;
4-Loder
1972)
Area
1.
2.
2:
5.
North central
Pacific
Ocean
Central
western
North Atlantic
Strait
of Georgia
(N. Pacific)
Chukchi Sea (Arctic
Ocean)
Diatom culture
Ocean
0.7%
1.5
13
24
72
ature of samples on 0.8-pm silver filters
( Selas Flotronics ) , As preparation, l-liter
samples were filtered on the Dawson cruise
and 5.5-liter samples were filtered on the
Sackville cruise. The filters had been
treated by baking at 500°C before samples
were collected. The analyses were done in
a carbon analyzer constructed by Wangersky (see Gordon 1969). Total organic carbon in O.l-ml samples of unfiltered seawater
and of filtrates was determined by combustion at high temperature ( Sharp 1973).
The filtrates were obtained by using Millipore filters of 25-nm pore size and Diaflo
membranes with 50,000 molecular weight
cutoff (Amicon Corp.), which have nominal pore sizes of 0.025 and 0.003 pm respectively. The 47-mm-diameter Millipore
filter was pretreated by boiling briefly in
distilled water (similar to the treatment
suggested by Nakajima and Nishizawa
1968). It was then placed in a Sterifil filter holder ( Millipore),
rinsed by filtering
100 ml of distilled water and 100 ml of
sample through it, and 30 ml of filtrate
were collected in a sample analysis bottle
(Sharp 1973). Filtration
was by vacuum
with a gauge pressure of minus 0.5 X 10” g
Diaflo memcm-“. The 76-mm-diameter
brane, in the model 400 ultrafiltration
cell,
had 100 ml of distilled water and 100 ml
of sample rinsed through it. Then 30 ml of
filtrate were collected in a sample analysis
bottle. Filtration was performed by pressure, with nitrogen at a gauge pressure of
5 x lo3 g cm-2. Carbon was analyzed directly from the sample analysis bottles.
ORGANIC
RESULTS
Particulate
AND
CARBON
DISCUSSION
organic carbon
The subject of particulate organic matter
in seawater has been reviewed recently
by Riley ( 1970); the discussion here pertains to particulate carbon values relative
to other fractions of the organic carbon
pool. Particulate organic carbon is often
considered to bc about 10% of the dissolved
organic fraction
(Parsons 1963). Early
work showed average values for particulate
organic carbon in the deep ocean of about
20-60 pg liter-l (e.g. Parsons and Strickland
1962; Menzel and Ryther 1964; Wangersky
and Gordon 1965; I-Iolm-IIansen
et al.
1966). More recent work shows deep ocean
averages closer to 10 pg liter-1 (e.g. Menzel
1967; Holm-Hansen 1969; Gordon 1971; this
work). Near surface values are more variable and less easy to compare, but they
were also probably overestimated in earlier work. The more recent values are lower
owing to more refined analytical procedures, less contamination in handling, and
better assessment of values for filter blanks.
Since the dissolved fraction is numerically close to that of the total organic carbon (see bdow ), it is permissible to interchange these two classes in the ensuing
discussion. In the subtropical North Pacific, Gordon ( 1971) found the particulate
to be about 1% of the total organic carbon,
He sampled seasonally from a single station at numerous depths. Table 1 lists some
values for the North Atlantic from the Sackville cruise. The SackviZZe data and data
from the Damon cruise are combined for
an average for the central western North
Atlantic Ocean (including
samples in the
Gulf Stream and the Caribbean).
This Atlantic average and Gordon’s Pacific average are listed in Table 2 along with an
average from seasonal sampling in a nearshore North Pacific region (Fulton et al.
1967) ; an average from sampling during
summer melt in the shallow, nearshore Arctic Ocean (Loder 1971) ; and an average
from a diatom culture in logarithmic growth
phase (Sharp 1972). I do not consider the
differences between the Atlantic and Pa-
IN
443
SEAWATER
TabZe 3. Four classesof organic carbon in
water samples. Station number and depth (in
are listed in sample column. Values in total
(0.8 pm)
umn are in mg C liter-l. Particulate
two colloidal
(0.025 and 0.003 f.hm) classes
listed as percents of total organic carbon
Percent
Sample
l-Sfc
4-Sf c
lo-Sfc
3-5
6-5
7-5
9-10
a-15
7-25
7-50
7-75
8-100
9-100
Total
urn
0.8
seam)
coland
are
of total
0.025
0.003
1.55
1.27
1.36
1.29
1.57
1.74
1.74
1. 44
1.49
I,.56
1.53.
2.4
2I4
2.1
2.3
2.8
1.9
2.4
2.4
3.1
2.4
2.2
4.7
13.2
6.2
8.1
5.1
3.3
18.8
9.0
16.6
1.09
1.38
1.9
11.9
22.9
2.2
2.2
1. 6
2.8
15.2
18.9
22.8
3-150
6-250
8-500
6-1000
9-1600
5-2000
2-4000
1.27
0.86
0.78
0.89
g-5100
1.08
1. LG
0.81
1.5l.
4.5
8.7
urn
28.4
15.8
14.0
3.1
10.8
9.8
26.9
1.0
1.6
1.7
0.3
1.2
urn
23.6
12.9
17.2
14.8
6.6
12.0
21.0
16.6
cific averages shown here to indicate real
regional
differences
between
the two
oceans. Table 2 illustrates the effect that
increasing phytoplankton
crop has on the
percentage of particulate
organic carbon
when oligotrophic
oceanic waters, eutrophic nearshore waters, and algal cultures
arc compared. This can also be seen in
comparing samples of deep water to the
samples of more shallow water (see Table
1) , In both cases, the increase is probably
due to detritus as well as living phytoplankton.
Clearly the particulate fraction
in oceanic waters is closer to 1% than the
often quoted 10, and, in deep water, is usually < 1%.
Only a portion of the particulate organic
carbon in seawater represents living matter
according to Riley ( 1959)) Mullin ( 1965b),
and Holm-Hansen ( 1969). Estimates from
their work show that in the near surface
waters about 10 to more than 50% of the
organic matter present is living.
Usually
less than 10% of the organic matter in deep
waters is living. Not only is a majority of
444
JONATHAN
H,
mg C/lltar
0:8
1.2
1.6
.
l ‘m*
l.
‘.
I
Fig. 1. Distribution
with depth of organic carbon. Data from Table 3, except that particulate
and colloidal classes are given as mg C liter-’ here.
Note broken axes.
the particulate matter not living, but also
the dissolved organic matter contains some
bacteria or bacterial pleomorphic
forms
(Anderson and Heffernan 1965; Sheldon
et al. 1967; Riley 1970). Different
size
groupings of particulate
organic matter
show increasing percentages of nonliving
matter within the smaller size groups ( Beers
and Stewart 1969).
Nonliving particulate organic matter has
been considered as food for filter-feeding
plankton (Raylor and Sutcliffe 1963; Riley
1970). It is undoubtedly also of importance
as surface for accumulation of both living
an d nonliving matter. However, as is discussed below, colloidal organic matter may
also be of importance in these two functions.
Colloidal
organic carbon
Colloidal matter consists of fine particles
in the approximate range of 0.001 to 1.0
pm, The oceanographer’s particulate cut-
SHARP
off of about 1 pm permits almost the entire range of colloidal matter to be included
in the dissolved class. For oceanic waters,
about 98% of the total organic carbon is
thus considered to be dissolved. Fox et
al. ( 1953)) using super-ccl cakes as “adsorbant” filters, concluded that colloidal
and particulate organic carbon accounted
for about 60% of the total organic carbon
in the sea, leaving the dissolved at about
40%. Ry modern analytical standards, their
carbon analyses were rather crude and
their estimate of colloidal matter is possibly
too high.
On the Damon cruise, I measured particulate organic carbon ( 0.8-pm cutoff),
the two classes of colloidal organic carbon
(0.025 and 0.003-pm cutoffs), and total
organic carbon. Subsamples of a single
sample were used for the analyses of the
four classes (Table 3). The four classes
were independently
assessed; the particulate and colloidal classes were cumulative
since each included everything larger than
its specific cutoff. Although the two types
of colloidal-cutoff
membranes behave in
different fashions (the 0.025 pm by physical exclusion and the 0.003 pm by molecular diffusion),
they respectively
retain
averages of about 10 and 20% of the total
organic carbon. This suggests that these
membranes are, in fact, performing
the
functions for which they were used; namely,
segregating colloidal organic matter. Figure 1 shows a composite depth plot of the
four classes of organic carbon from the
Dawson cruise, The somewhat unusual distribution of total organic carbon is due to
the analysis having been made by high
temperature combustion rather than by
chemical oxidation ( Sharp 1973). The two
colloidal classes have a somewhat different
distribution
from either the total or the
particulate class.
When the particulate
fraction is subtracted from the colloidal ones, an average
of 8% of the total organic carbon is in the
range of 0.025-0.8 pm and 16% is in the
range of 0.003-0.8 pm. Ogura ( 1970), with
a somewhat similar procedure, found 7%
ORGANIC
CARBON
of the total organic carbon in the range of
0.1 to 0.45 pm.
The methods used here for segregating
colloidal matter are not well established
and the definition of colloidal matter itself could be challenged. However, it is
estimated that the colloidal organic carbon
class is about 10 times the size of the par(1965n) found the
ticulatc class. Mullin
majority of the particulate organic carbon
in his Indian Ocean samples in the smallest size classes that he examined. Converting his values into cumulative percent of
total organic carbon (using a particulate
estimate of 2%, as in Table 3), I have calculated a size distribution
of organic carbon in seawater which includes the colloidal classes (Fig. 2). The increase in
amount of organic carbon with decreasing
particle size extends into the colloidal range.
Also, it is obvious that the colloidal matter
is far more abundant, by weight, than the
particulate.
In fact, Reiswig (1972) has
suggested that much of the particulate
matter is probably colloidal also.
Colloidal organic matter may be of considcrablc ecological importance as well as
of quantitative
significance.
The hypothcsis that fine colloidal matter can be used
as food for some marine organisms (MacGinitie 1945; Fox et al. 1953) has not been
well tested. .Bcers and Stewart ( 1967, 1971)
have suggested that the microzooplanktcrs,
many of which are protozoans, have a more
profound role in the marine food chain
than has been attributed to them. Fecding habits of these organisms are poorly
understood. Any that might utilize mucoid
surfaces, alone or in conjunction with cilia
or pseudopoda, could capture fine colloidal
particles. Recently two pelagic macrozooplankters have been shown to use mucoid
webs for food capture (Gilmer
1972).
Neither the relative abundance of zooplankters that capture food on mucoid surfaces
nor the possible size limitations
of matter captured by such organisms has been
investigated.
Colloidal organic matter may also be of
importance in chelation of heavy metals;
IN
445
SEAWATER
IO3
IO2
h
E IO’
V1,
Q)
N
.UY
a
IO0
0
.+
L
Lt
10-l
IO
-2
IO-?
i
F;
I;
1’6
% of Tot al
Organic
Carbon
kumulotive)
Fig. 2. Generalized
size distribution
of organic
carbon in seawater.
Based on values from Table
3; sizes above 1 pm are from MulIin
(19&S),
fitted to data from Table 3.
Barber (personal communication),
using
ultrafiltration
methods similar to those dcscribed above, illustrated what appears to
be chelation ability in the matter removed
by the ultrafiltration
membrane. It may also
be important as a source for formation of
particulate organic matter in seawater, as
was suggested by Wangersky (1965) and
demonstrated by Sharp ( 1972).
446
JONATHAN
Preliminary
data on the abundance of
colloidal organic carbon has been given
here for the central western North Atlantic
Ocean,
More quantitative
information
about this class is needed. From the data
available, it appears that the distribution
of colloidal organic carbon with depth is
unlike that either of particulate or of total
organic carbon. The amounts of organic
carbon in different size classes (as illustrated in Fig. 2) suggest that a smooth
continuum might exist from truly dissolved
molecules through large particles. Along
with such a continuum, a constant breakdown and formation of various size groupings may occur. Further investigation
of
distribution could provide some ideas about
origin and utilization
of colloidal organic
matter.
Since almost all ( > 95%) organic carbon
in oceanic waters is in the dissolved class,
and since this class is incorrectly defined,
it should be abandoned in routine carbon
analysis.
Instead, total organic carbon
should be considered. Similarly, the practice of routine measurement of particulate
organic carbon should be reevaluated in
light of the demonstration of a considerably larger class which is considered here
as colloidal.
Qualitative
work on colloidal organic
matter should be a fruitful line for research.
Preliminary
investigations
indicate
that
some labile colloidal protein can be found
in seawater (Sharp, unpublished
data),
which might be used for food by zooplankton if it could be ingested by them. This
class of organic matter might also prove
interesting for other studies of extra-organismic -biochemistry,
such as free enzymes in seawater. It is apparent that the
tools we have available in ultrafiltration
equipment could open new horizons in
marine organic chemistry.
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Submitted: 9 October 1972
Accepted: 29 January 1973