Limnol.
Oceanogr., 34(l), 1989, 163-177
0 1989, by the American Society of Limnology
and Oceanography,
Inc.
,
Protozoans in two southeastern blackwater rivers and
their importance to trophic transfer
Leslie A. Carlough and Judy L. Meyer
Institute
of Ecology and Department
of Zoology,
University
of Georgia, Athens 30602
Abstract
Protozoan population densities in the sixth-order Ogeechee River and fourth-order Black Creek
ranged from 6 x lo4 to 11 x 10” flagellates liter-l and 0 to 1.5 x lo5 ciliates liter-’ over a 12month period. These numbers approximate
those reported for various marine and freshwater
habitats. A microcosm study with Ogeechee River water showed a density increase from 4 x lo5
to 9 x lo6 flagellates liter -I and 7 x 10) to 4 x lo5 ciliates liter-’ in 2 d, representing an estimated
net protozoan production of 600 pg C liter -I d-l. This production was mainly attributed to bacterial
growth on DOC and subsequent grazing by the protozoans. Although problems always accompany
container studies, this indicates an immense potential for protozoan production in the river. Daily
transport of protozoan carbon ranged from 1.08 to 1,360 g, and annual estimated transport downstream was 60 t of protozoan carbon in the Ogeechee River. Densities of filter-feeding macroinvertebrates are very high in this river. Many of the filter-feeding species are known to feed primarily
on amorphous material in the seston, within which protozoans consitute about 4% by carbon
content. Since protozoans can be assimilated at relatively high efficiency (-50%), they appear to
bc a trophic link between the metazoans and otherwise unavailable carbon sources in blackwater
rivers.
energy, hinges on the efficiency of the microorganisms,
the number of microbial
trophic levels involved, and their residence
time in the water column. The question remains unanswered (Ducklow et al. 1986,
1987; Sherr et al. 1987).
Before we can determine whether protozoans are a link between bacteria and higher
trophic levels in stream ecosystems, we need
to know their numbers and biomass in these
environments. Here, the term “protozoan”
includes Ciliophora
(ciliates) and Sarcomastigophora
(pigmented flagellates, colorless flagellates, and ameobae) and should
not be taken to represent a true taxon (Lee
et al. 1985).
Our objective here was to quantify protozoan abundance in main-channel
and
backwater habitats of a blackwater river and
examine the temporal variability on scales
of 1 d, 2 weeks, and 1 yr. A microcosm
experiment was also performed to estimate
the potential protozoan production within
a parcel of water as it flows downstream.
Protozoan density and biomass from this
Acknowledgments
river were compared to other, more freThis research was supported by National Science
Foundation grants BSR 84-0663 1 and BSR 87-05744
quently studied ecosystems. Our intent was
to J. L. Meyer. We are especially grateful to R. W.
to assess the potential importance of proSanders and R. T. Edwards for lab and field assistance.
tozoans as a food resource for the abundant
The manuscript benefited from the comments of K. G.
filter-feeding
invertebrates
in the river
Porter, L. R. Pomeroy, R. T. Edwards, G. M. Capriulo,
and an anonymous reviewer.
(Wallace et al. 1987; Benke and Meyer 1988)
163
The protozoans of lotic ecosystems have
received little attention. During the 196Os,
extensive surveys of epibenthic stream protozoans addressed patterns of diversity and
succession with great taxonomic
detail
(Cairns 1965, 197 1); however, protozoan
population densities, biomass, or production were not estimated, and their importance in the trophic structure of rivers was
not examined.
Much of the ecological work on protozoans has been done in marine systems or
on laboratory cultures of freshwater forms.
Early work showing that much of the energy
fixed by photosynthesis is used by protozoans (Pomeroy and Johannes 1968) led
Pomeroy (1974) to suggest that, in addition
to the classical algae-herbivore-carnivore
food chain, there may be a “microbial loop”
that funnels bacterial production back into
the classical web via protozoans. Whether
this microbial loop is truly a link or whether
it acts as a sink, burning off carbon and
164
Carlough
Fig. 1. Map showing the locations of sampling sites
on the Ogcechee River and its tributary, Black Creek.
Inset shows the location of these streams.
as part of a research project on the food webs
of the Ogeechee River and its tributary,
Black Creek.
Study sites
The Ogeechee River is located on the
Georgia Coastal Plain and drains into the
Atlantic Ocean near Savannah. Black Creek
is a fourth-order tributary of the sixth-order
Ogeechee River. Both of these rivers are of
low gradient (0.02%), and the predominant
main-channel substrate type is sand (0.3%
organic matter, Findlay and Meyer 1984)
with mud (0.05-56% organic matter, FindBay et al. 1986b) in the backwater areas. Because these rivers drain the coastal plain
they are high in humic and fulvic substances
and the water is darkly stained. Dissolved
organic carbon concentrations are higher in
Black Creek (mean: 3 1.8 mg C liter-l; range:
5.2-74) than the Ogeechee River (mean: 13.5
mg C liter-‘; range: 4.4-34, Meyer 1986).
The average temperature is 18.5”C but varies from 7” to >30°C over the year with a
pH range of 5.5-7.5 (Meyer 1986). More
detail about the physical and chemical characteristics of the Ogeechee River is given
and Meyer
elsewhere (Wallace and Benke 1984; Benke
and Meyer 1988).
Accompanying the runoff of dissolved organic substances are many bacteria. As a
result, both the Ogeechee River and Black
Creek have high suspended bacterial biomass: bacterial density ranges from lo9 to
10” cells liter-’ with a mean of 1.5 x lOlo
(Edwards 1985, 1987). Many of these bacteria seem to be inactive soil bacteria, since
bacterial production is lowest when the river is flooding and bacterial biomass is highest (Ogeechee River: 0.058-2.120 mg C m-3
h-l; Black Creek: 0.002-2.418 mg C m-s
h-l; Edwards and Meyer 1986). Dense populations of filter-feeding
macroinvertebrates inhabit the abundant woody debris
(snags) in the channel; for every 2-l 2 m2 of
sediment surface, there is another 1 rn” of
surface area in snags (Wallace and Benke
1984). Filter-feeding
macroinvertebrates
number -20,000 individuals
m-2 of snag
surface in the Ogeechee River (5,500 ind.
m-2 of bed surface area) (Wallace and Benke
1984).
Three sampling sites were chosen from
the two rivers (Fig. 1): one main-channel
site from the Ogeechee River, one mainchannel site from Black Creek about 2 km
above its confluence with the Ogeechee River, and a backwater site adjacent to, but
opening downstream from, the Black Creek
main-channel site.
Methods
Routine sampling-Two
samples were
collected monthly from April 1984 to March
1985 from the three sites by submerging two
bottles containing Lugol’s iodine acid fixative-stain (1% final concn; Taylor 1976; Sieburth et al. 1978) to a depth of 0.5 m and
allowing them to almost fill. They were assumed to be typical of the whole water column as the flow is turbulent and the water
well mixed. The samples were stored in the
collection bottles at room temperature in
the dark. Temperature was taken at each
site, and river discharge was obtained from
a LJSGS monitoring station at nearby Eden,
Georgia.
Comparison of jxation
techniques- We
used Lugol’s acid stain to preserve the protozoans because it has been extensively used
Protozoan;
in blackwater rivers
in other protozoan studies (Capriulo and
Carpenter 1980; Smetacek 198 1; Gates
1984; and others) and because it is inexpensive, easy to use in the field, and samples
thus treated have been preserved effectively
for B-10 yr (Taylor 1976). Lugol’s is better
than most preservatives for naked flagellates because it helps to retain flagella (Taylor 1976), resulting in “. . . the best result
from a combined qualitative and quantitative view” (Throndsen 1978, p. 73). Although formaldehyde
has been the most
commonly used preservative, it has also
been criticized for use on natural populations or for biomass estimations (Sorokin
1981; Throndsen
1978). Sieburth et al.
( 1978) maintained that Lugol’s and Formalin are both “suitable” for preservation
of naked and unarmored phytoplankton and
protozooplankton.
A comparison was made between counts
with Lugol’s at 400 x and a newer technique
with the epifluorescent stain primulin (Caron 1983) at 1,200 x . Two subsamples were
taken from each of two samples: a dense
backwater sample having much amorphous
particulate matter, and a rather depauperate
main-channel sample. One subsample was
preserved with 1% Lugol’s and counted as
described below, and the other was preserved with 4% gluteraldehyde buffered with
0.2 M NaH,PO, and stained overnight with
250 pg ml- l primulin. Subsamples were filtered onto 0.8-pm pore-size filters and
counted at 1,200 x . The estimated densities
were very close for both samples with both
methods, though the Lugol’s technique
showed the higher estimates (the ratio of
total flagellates with Lugol’s to that with
primulin was 1.06 for the backwater and
1.19 for the main-channel).
Protozoan counting procedures and biomass estimation -After
gently remixing
each bottle by inversion, a 50-ml subsample
was placed in a graduated glass cylinder.
The particles were allowed to settle (3 h
cm-’ of column ht; Utermijhl
1958), at
which time the top 45 ml were aspirated
away. The sample was resuspended, placed
in a lo-ml settling chamber, and allowed to
settle in an insulated box for at least 24 h
before counting on an inverted microscope
(Zeiss 30 IM) with transmitted illumina-
165
tion. Counts were done at 400x, as this
magnification
still permits observation of
the smallest flagellates (Sorokin 198 1; Smetacek 198 1; Fenchel 1982). Phase-contrast
microscopy was not used because distortion
by detritus and suspended sediments made
identification
of flagella or cilia difficult. A
randomly placed 0.3-mm-broad
transect
was projected through the center of the
chamber. With few exceptions, at least 300
individuals were enumerated from two subsamples for each of the two samples. The
difference in counts between the two subsamples averaged 16% of the mean (SD
10%). The difference between the two sample bottles averaged 19% of the mean (SD
14%).
A disadvantage of Lugol’s and transmission microscopy is that pigmented and nonpigmented forms are not distinguished. Even
those with pigments, however, may also be
bacterial consumers (Porter et al. 1985).
Therefore, we counted all motile protozoans (having flagella, cilia, pseudopodia)
because they are the most likely to be active
bacterivores. Protozoans were separated into
four categories: flagellates ~6 pm in largest
dimension, flagellates > 6 pm but < 15 pm
in largest dimension, flagellates > 15 pm,
and ciliates. Groups or morphs that were
particularly dense in each sample were enumcrated separately. In addition, flagellates
> 15 pm and all ciliates were measured for
length and width. Ameobae were very rare
and were treated in the same manner as
ciliates.
We estimated protozoan carbon using the
length and width for the size classes and
number of individuals
in each size class.
Biovolumes
were estimated
as prolate
spheroids for all ciliates (Gates 1984) and
an egg-shape for all flagellates. Biovolumes
were converted to carbon assuming protozoan specific gravity equals 1.O (Sherr and
Sherr 1984), dry weight is 20% of wet weight,
and carbon is 40% of the dry weight fraction
(Beers and Stewart 1979). This latter estimate is probably conservative as Finlay and
Uhlig (198 1) noted that only protozoans
with a very unusual chemical composition
could have a carbon content (as % ash-free
dry wt) <40%. The resultant coefficient used
to estimate protozoan carbon from volume
166
Carlough
is within the range used by others (Carlough
1987). The estimated carbon concentrations in each size class were summed and
multiplied by the daily mean discharge to
estimate total protozoan carbon transported
at the Ogeechee River and Black Creek
main-channel sites.
Bacterial counting procedures and biomass estimation -Bacterial
population
densities were determined by an acridineorange direct-counting
(AODC) protocol
(Hobbie et al. 1977) after removing the iodine color with Na2S203 (Pomroy 1984;
Nishino 1986). Detailed procedures are described by Carlough (1987). Counts were
made on an Olympus BH-2 microscope with
a mercury lamp. Bacteria were counted into
three categories: cocci <0.2-pm diameter
(minibacteria),
cocci >0.2 pm, and rods.
Bacterial numbers were converted to biomass with conversion factors derived previously (Edwards 1987) for the Ogeechee
River (cocci, 0.064 pm3; rods, 0.176 pm’)
and Black Creek (cocci, 0.023 pm3; rods,
0.093 pm3). Volumes for the minibacteria
were derived by assuming the cells to be
spherical with a diameter of 0.15 pm (volume equals 1.8 x 1Op3pm3). Bacterial carbon content was estimated assuming 2.2 x
IO-l3 g C prnm3 bacteria (Bratbak and Dundas 1984).
The rank correlation coefficients, Spearman’s r,, and Kendall’s 7 were calculated to
measure the strength of relationship
betwcen the various protozoan and bacterial
categories, discharge, and temperature.
Microcosm experiment and intensive river
sampling-A
200-liter plastic garbage can
was filled with main-channel Ogeechce River water at 1000 hours on 20 August 1985.
The can was suspended in a large innertube
and anchored at the surface of the river to
keep it at ambient temperature. The water
in the microcosm was mixed with a continuously operating gear-motor turning a propeller at 0.28 rps. Mixing from surface to
bottom took 30 s.
Protozoan samples from the microcosm
and the Ogeechee River main-channel and
bacterial samples from the microcosm were
taken concurrently every 4 h for the first
day with the collection and enumeration
methods described previously. After the first
and Meyer
24 h, bacterial and protozoan samples were
taken daily at 1000 hours. Sampling continued for 3 d from the microcosm and for
14 d from the river. Samples for dissolved
organic carbon (DOC) analysis were also
taken from the river daily. DOC was analyzed on a Dohrman DC 54 carbon analyzer, which uses UV-catalyzed
oxidation in
the presence of persulfate. Rainfall and river
height were documented daily.
Results
Species composition-Changes
in protozoan diversity and community
structure
were very rapid (Carlough in press). Although it was not possible to do a complete
taxonomic analysis of the species encountcred concurrently with counts for density
and biomass estimates, some taxa were
commonly found. Most of the smaller flagellates were difficult to identify, but included species of bodonids and monads and
Spermatozopsis. The larger flagellates consisted in part of cryptomonads (Cryptomonas, Chroomonas, Chilomonas), the dinoflagellate Glenodinium, various unidentified
chlamydemonads,
and euglenoids
(Euglena, Distigma, Phacus). Several colonies
of Volvox, Eudorina, and Dinobryon were
seen. Sarcodinids were very rare but included Dtflugia,
a single heliozoan (Actinospherium), and a single unidentified naked ameoba. Ciliates consisted mostly of
Halteria (an oligotrich) and a species of the
family Cyttarocylididac
(a choreotrich).
Others include stichotrichs, colpodids, and
unidentified species.
Seasonal study: Black Creek backwater
site-- Protozoan population densities in the
back.water area varied widely over the year.
Populations during summer were generally
denser than those of fall and winter (Figs.
2a, 3a), but blooms were also seen in midfall
and spring. Flagellates were highest in March
1985 with a density of 6.4 x lo6 ind. liter-’
(0.49 mg C liter-l), whereas ciliates were at
their peak density in June 1984 with 5.2 x
lo4 ind. liter-’ and at peak biomass in September (0.040 mg C liter’).
In a preliminary sampling during September 1983,3.02
x lo5 ciliates liter-l were found at this site.
Flagellates constituted the greatest percentage of the protozoans, accounting for 98%
Protozoans
167
in blackwater rivers
IO’ - W
‘j.=!
&
a lo-‘s
s
0” 10-3’
F
1o-5!
IO3
Month
Fig. 2. Monthly numerical abundance of bacteria
(O), flagellates (Cl), and ciliates (A), April 1984 through
March 1985. The range and mean of two samples are
plotted for each date; the range is within the area of
the symbol for many dates. Only one sample is reported
for the flagellates and ciliates during February and
March. Where the lines leave the graph, densities were
too low to be measured accurately. a-Black
Creek
backwater; b-Black
Creek main-channel;
c- Ogeethee River main-channel.
of total abundance and 86% of estimated
biomass.
Flagellate density and biomass were significantly correlated (a, = 0.05) with the densities of all categories of bacteria; ciliate
!
!
A’M’J’J
Fig. 3.
!
!
!
!
!
!
!
!
!
!
!
‘A’S’O’N’D’J’F’M’A’
Month
As Fig. 2, but of biomass.
density and biomass were correlated with
cocci and total bacterial density. Flagellate
and ciliate densities and biomasses were significantly
correlated. Ciliate density and
biomass were significantly related to temperature.
Seasonal study: Black Creek main-channel site- The tremendous increases and decreases typical of the backwater site were
not evident (Figs. 2b, 3b) at the main-channel site. As in the backwater site, densities
were high in summer and lower in fall and
268
Carlough
Table 1. A summary of the protozoan carbon transported downstream daily in the Ogeechec River as a
function of rate of discharge and protozoan carbon
concentration on that day.
and Meyer
downstream transport of >64 t of protozoan carbon. It may be an important input
of high-quality
carbon to the downstream
estuary. Although the densities and bio1984-1985
(m’ s-l)
(jog C liter-‘)
(kg C d -‘)
masses of flagellates and ciliates were significantly correlated (a := 0.05), they were
20 Apr
128
1.04
11.5
20 May
82.0
2.89
20.4
not correlated with any bacterial fraction or
21 Jun
15.6
4.35
5.87
with temperature or discharge.
23 Jul
24.2
8.83
18.5
Microcosm experiment -After initial de11 scp
11.4
1.02
1.01
creases
in bacteria, flagellates, and ciliates,
5 Ott
9.26
11.00
8.80
all began to increase by the end of day 1
17 Nov
10.4
2.93
2.65
4.73
25 Jan
23.0
9.41
(Fig. 4a). Bacterial density peaked (4.5 x
22.5
320
21 Feb
165
1O1cL
cells liter-‘) at this time. Abundance of
29 Mar
438
1,380
36.5
flagellates (9.3 x 10” ind. liter-l) and ciliate
Annual mean
49.7
177
50.5
density (3.8 x 1O5 ind. liter-l) peaked after
2 d. As the protozoans were increasing, bacterial density decreased to half its maximal
winter. No fall bloom was seen, but a large level by the end of the day 3. During the
bloom was noted in spring. Flagellates were microcosm experiment, the densities of flathe dominant protozoans, accounting for gellates and ciliates and ciliates and bacteria
98% of total abundance and 87% of esti- were significantly correlated (Table 2).
rnated biomass. Flagellate density and bioIntensive river sampling- Discharge demass were highest in March 1985 (1.1 x creased from 27.7 to 14.4 m3 s-l during the
lo7 ind. liter-‘, 0.83 mg C liter-l). Ciliate
first 4 d, then increased steadily to 8 1 m3
density was highest in February (1.3 x 1O4 s-l on day 13. DOC concentration
flucind. liter-‘, 1.7 pg C liter-‘). Mean daily
tuated similarly; it decreased from 24 ppm
carbon transport was 5.06 kg (range, 14.0 to 13 over the first 5 d, then increased to
g-46.9 kg).
43 on day 13. Both bacterial and flagellate
Flagellate and ciliate densities and flageldensities increased rapidly during the first
late biomass and temperature were signifiday and then showed a slower increase until
cantly correlated (a = 0.05). Neither ciliate
about day 8 (Fig. 4b). Between days 8 and
density or biomass nor flagellate density or 11, both bacteria and flagellates decreased,
but. within 3 d regained their former denbiomass were significantly correlated with
sities and peaked again. Ciliates showed less
any bacterial fraction or with river dispattern but increased over the 2-week pecharge.
riod.
Seasonal study: Ogeechee River mainFlagellate, ciliate, and bacterial densities
channel site-Protozoan
densities in the
Ogeechce River showed a pattern similar to were all significantly correlated. Each was
that at the other two sites (Figs. 2c, 3~). also significantly correlated with DOC and
two measures of river discharge (Table 2).
Densities were highest during the spring
bloom, with generally lower abundances in
late fall and winter. As at the Black Creek Discussion
Protozoan communities: Patterns of rapid
main-channel site, no bloom occurred in the
the 2-week infall. Flagellates accounted for 99% of the change in density-During
total protozoan abundance and 85% of the tensive sampling, we found significant corestimated biomass. Flagellate densities and relations between flagellate densities, ciliate
biomass were highest in March (1.1 x lo7 densities, and bacterial abundance (Table
correlated
ind. liter-‘, 0.40 mg C liter-l). The high for 2). All these were significantly
ciliate density and biomass was also in with DOC and river discharge. Thus it would
appear, at least over the short term, that
March (1.5 x 1O5ind. liter-l, 27 pg C liter-‘)
relationships
between protozoans
and
(Figs. 2c, 3~). Mean daily carbon transport
was 177 kg (range, l.Ol-1,380 kg: Table l), changing physical parameters can be resolved (Bark 198 1). However, it should be
which translates into an estimated annual
Protozoans in blackwater
169
rivers
Table 2. Spearman’s rF rank coefficients of correlation for the microcosm and intensive river study.
Coefficients calculated with Kendall’s T rank correlation yield similar results. Sample n: 9-microcosm;
20 -intensive
river study biological correlations; 15 intensive river study correlations with physical parameters. (Asterisks: *- significant at a! = 0.05; **-significant at a = 0.0 1.)
Flagellate
density
IO3
!
I
I
I
I
I
I
I
0
2
4
6
8
10
12
14
Day
Fig. 4. The densities of bacteria (O), flagellates (Cl),
and ciliates (A) sampled over a 3-d period for the microcosm (a) and a 2-week period for the Ogccchee River main-channel (b).
noted that a positive correlation between
two time series arises whenever the trend
in both parameters is in the same direction.
This type of increase was seen in the microcosm and the in situ study (Fig. 4).
When monthly samples were taken for a
year, fluctuations in protozoan density, carbon, and protozoan carbon transport occurred in the three habitats (Figs. 2 and 3).
In this longer term study, flagellate and ciliate densities were significantly correlated,
however, none of the protozoan parameters
were significantly correlated with bacterial
abundance, tcmpcrature, or discharge for all
three sites.
Similar fluctuations in protozoan density
were found by Taguchi ( 1976), who sampled protozoans monthly for a year in a bay
in Japan. He found that densities were generally highest in late spring and summer and
Ciliate
density
Microcosm
Ciliate density
Bacterial density
0.929**
0.545
0.700*
Intensive river study
Ciliate density
Bacterial density
DOC
Daily discharge
Rate of change in discharge
0.721**
0.910**
0.612*
0.746**
0.746””
0.593**
0.769**
0.895**
0.895**
lowest in late fall and winter. Other researchers have noted similar patterns of
protozoan density (Gates 1984; Beers et al.
1980; Eriksson et al. 1977).
As demonstrated by the microcosm experiment, rapid change can occur not only
at a site, but within a water parcel as it moves
downstream. Although the microcosm initially contained the same numbers of bacteria and protozoans as the river, changes
were more rapid in the microcosm (Fig. 4a,
b). A bacterial bloom on day 1 preceded a
protozoan bloom and a rapid bacterial decline by the end of day 2. Similar sequences
of events are commonly reported from other systems (Linley and Newell 1984; Andersen and Fenchel 1985) and have been
noted in the Ogeechee River (Findlay et al.
1986a). However, this microcosm was not
replicated; results should therefore be interpreted with caution.
We calculated a rough grazing rate for the
flagellates feeding on bacteria [grazing rate
(cells liter-’ h-‘) = flagellates (ind. liter-l)
x clearance rate (liters ind.-’ h-l) x bacterial concentration (cells liter-l)]. Using a
midrange clearance rate estimate of 1O-s liters flagellate- 1 h-l (Anderson and Fenchel
1985) and the densities of the bacteria and
flagellates at the time of the bacterial peak
produces a grazing rate of 1.O x lo9 cells
liter-’ h-’ . It would be great enough to prevent increases in bacterial density even
though the bacterial doubling time was about
170
Carlough
and Meyer
Table 3. Statistical descriptions of annual protozoan densities (lo6 liter-‘) and biomass (pg C liter-‘) in the
Black Creek backwater site, the Black Creek main-channel site, and the Ogeechee River main-channel
site.
Calculations are based on 10 sample dates. The C.V. is reported as SE divided by the mean.
Black Creek backwater
Black Creek main-channel
Ogeechee River main-channel
I .9(0.07 l-6.4)
1.5(0.058-I 1)
1.9(0.066-l 1)
2 h at the time of the peak. This grazing
estimate is high because of the assumption
that most protozoans are predatory and that
both pigmented and unpigmented protozoans are bacterivorous,
but pigmented
protozoans are a small fraction of the community: 2% in July 1986 (Carlough 1987)
and 2-6% in November 1986 (B. Miller
pers. comm.). Although we don’t know the
annual variation
in percent autotrophs,
chlorophyll concentrations in the river are
very low throughout
the year (Edwards
1985); hence the percentage of autotrophs
is also expected to remain low. Therefore,
the grazing rate estimate indicates that protozoan grazing was responsible for the bacterial decline in the microcosm, implying
that protozoan grazing is a potentially significant source of bacterial mortality in the
river.
Fallon et al. (1986) showed that in a coastal estuary with tidal flooding, protozoans
and bacteria cycle out of phase on an 81O-d cycle; Fenchel ( 1982) found similar
asynchronous cycling with a 16-d frequency
in a North Sea sound. During our intensive
study, no such cycling was apparent over
the 2-week period in the Ogeechee River
(Fig. 4). This might seem paradoxical to the
hypothesis that protozoans control bacterial
densities; however, such close coupling of
protozoan and bacterial densities in lotic
systems is confounded by six factors. There
are time lags between prey increases and
predator response (e.g. Fig. 4a). Trophic interactions between bacteria and protozoans
can be in part suppressive, in part supportive (Johannes 1965; Banoub and Williams
1973; Sieburth et al. 1978). Complex interactions exist between different guilds in the
microbial food web (Rassoulzadegan and
Sheldon 1986). Turbulence in the river will
result in suspension of benthic bacteria and
0.38
0.71
0.56
162( 1.O-590)
94( 1.2-830)
49(1.1-430)
0.43
0.87
0.82
protozoans. Benthic filter-feeding metazoans will graze on both bacteria and protozoans. Because the river is a moving water
column, a sample taken from it on a given
day is not from the same mix of source areas
as a sample taken on a later day.
Comparisons between sites -The average
densities for the three sites were similar, but
the Black Creek backwater had three times
the protozoan biomass of the Ogeechee site
(Table 3). This disparity occurred because
the main-channel sites, especially the Ogeethee River, had proportionally
fewer of the
larger bloom forms (Carlough in press). The
Ogeechee River has a greater current velocity, volume, and higher order. The history
of its water is more complex, including the
input of a greater number and diversity of
tributaries and backwaters. A bloom species
in the Ogeechee River will therefore be diluted faster and have more competitors,
making it more difficult to establish a bloom
population.
Comparisons with other environmentsProtozoan densities in the Ogeechee River
ranged from 5 x 1O4to 11 x lo6 flagellates
liter-l and 6 x lo2 to 15 x 1O4 ciliates
liter’.
The backwater site had up to 3.02
x 105 ciliates liter-‘, one of the highest densities reported for any natural aquatic environment, Comparisons with densities in
other environments
are difficult because
there is no standard protocol either for stain,
type of microscopy,
or the taxonomic
groupings used in counting. Since many of
the studies do not cover seasonal differences
and may not include annual density maxima, comparisons are further complicated.
We have compared Black Creek and Ogeethee River ciliates and flagellates with other
environments (Tables 4 and 5). Only those
studies purporting to report complete assemblages were included. Because many re-
Protozoans
in blackwater rivers
searchers reported only maxima, we have
ranked the densities by the maximum reported value.
Among the studies of ciliates in various
aquatic environments
including
coastal,
open ocean, lake, and river sites (Table 4),
the Ogeechee River main channel ranked
near 90%. The Black Creek main-channel
site ranked near the 50th percentile. The
Black Creek backwater site had a greater
density of ciliates than 96% of the published
studies. All three of these blackwater sites
ranked considerably higher than the only
two other river sites reported. They were a
cold, fast-flowing river (Bereczky 1980) and
an English chalk stream (Baldock et al.
1983). Fewer studies of densities of natural
flagellate assemblages were found. Of the
studies included (Table 5), the Black Creek
backwater site ranked near the 70th percentile, while the main-channel sites were 2 90%
of the reported flagellate densities.
Porter et al. (1985) related ciliate density
to Chl a concentration in 41 lakes ranging
from oligotrophic
to hypereutrophic.
The
Ogeechee River has higher ciliate abundance for its chlorophyll
level than predicted by a regression developed from these
lakes (Fig. 5a) and slightly lower biomass
(Fig. 5b). A reason for the high abundance
of smaller ciliates in the Ogeechee River
relative to its chlorophyll
content may be
that the larger ciliate species that specilize
on phytoplankton
are missing as a result of
the low concentrations of algae.
Protozoans and thefood web of blackwater
rivers-In
the Ogeechee River allochthonous and autochthonous DOC is taken up
and turned into free and attached bacterial
biomass with an efficiency of 30-50% (Findlay et al. 1986a; Meyer et al. 1987). Protozoan response to increases in bacteria is
rapid (Findlay et al. 1986a). In the microcosm experiment described here, bacterial
growth preceded a period of high protozoan
production. It is not possible to estimate the
biomass of bacteria consumed from these
data since the efficiency of conversion of
bacterial biomass to protozoan biomass
ranges widely from 0.37 to 0.78 and depends on various biological, chemical, and
physical factors (Curds and Bazin 1977). Nor
is it feasible to determine the gross proto-
171
zoan production because it is difficult to
measure mortality. Average net flagellate
and ciliate production,
however, is estimated to be 600 pg C liter-’ d-l for this 2-d
period of rapid growth.
The most likely consumers of protozoans
are the abundant macroinvertebrate
filter
feeders found on snags. Gut analyses of
dominant filter-feeding insect species able
to retain particles 5 10 pm in the Ogeechee
River showed that 94-98% of the food in
the foregut is amorphous material (AM)
(Wallace et al. 1987). Even in the larvae
which have a large mesh size and specialize
on animal drift, AM accounted for 43-62%
of the total foregut volume (Wallace et al.
1987). AM is a catch-all category for items
that cannot be identified as animal, vascular
plant, fungi, diatom, or “other algae.” It
includes feces, flocculated DOC, bacterial
aggregates, free bacteria, and protozoans. In
the gut contents of copepods, amorphous
material has been assumed to be of flagellate
origin (Porter 19733) or ciliates (Porter
1973a).
We made estimates of the potential contribution of protozoan carbon to the AM
pool with data from Edwards ( 1987) and
this study. Of the total seston carbon in the
Ogeechee River, 3 1% (range 8-52%) was estimated to be bacterial biomass based on
nine monthly samples taken in 1983-l 984
(Edwards 1987). The annual average ratio
of protozoan carbon to bacterial carbon was
0.125 (range, 0.002-I .22) during 1984-l 985
(Carlough 1987). Combining
these estimates from different years, we calculate that
protozoan and bacterial carbon constitute
an average of 35% of the total seston carbon
in the Ogeechee River. Since an average of
83% of the total seston carbon is AM (Wallace et al. 1987), protozoans and bacteria
could account for about 42% of the AM in
the Ogeechee River. Although crude, this
estimate demonstrates the potential importance of the living material in the amorphous fraction of the seston.
Studies of assimilation efficiencies of food
particles tend to estimate detrital assimilation by aquatic invertebrates to be only
about 5% (e.g. Benke and Wallace 1980)
based mainly on ingestion of sediment and
vascular plant detritus, which contain much
172
Carlough
and Meyer
Table 4. Literature values of the population densities of natural ciliate assemblages. O-Oligotrophic;
Eeutrophic; M-mesotrophic.
Values are ranked from lowest to highest based on the maximal reported density.
(X 10’ liter-‘)
0.004-0.5
0.7
O-l .4
0.7-I .4
1.5
1.9
0.7-2.0
3.3
0.45-3.7
4.3
4.4
5.2
5.8
6.0
6 max
6.2
0.5-6.3
6.7
7
O-8.0
0.5-8.0
8.5
7.2-8.7
8.8
2.2-8.8
O-9.0
9
0.02-9.1
0.3-9.1
0.1-10
0.1-10
O-10.3
l-10.5
0.08-10.6
10.8
0,034-l 2.5
0.4-12.5
2.0-l 3
13.8
2.2-14.7
15.0
17
17.1
17.8
19
9-19
19.2
20.1
21.6
22
6.0-23
23.5
27.5
27.9
28.4
28.8
29
30
5 .o-30
30
Environment
and description
Danube, Hungary (cold, fast river)
River Frome, U.K. (chalk stream)
Gulf of Maine
Pacific Ocean, north central gyre
South Pacific Ocean, Tradewinds
Ivan’kovsky,
USSR, 0
Pacific Ocean, tropical
Lake Bowker, Quebec, 0
Black Sea
Lake Orford, Quebec, 0
Lake Brompton, Quebec, 0
Bauline Long Pond, Newfoundland,
0
Lake Brome, Quebec, E
Lake Lovering, Quebec, 0
Akkeshi Bay, Japan
Bothnian Sea, Sweden
Gor’kiy Prov. lakes, USSR, 0
Lake Argent, Quebec, M
Pacific Ocean, equatorial divergence
Univ. Penn. botanical pond, Pennsylvania,
Lake Mikolajskie,
Poland, E
Lake Masawippi, Quebec, E
Lake Mephremagog, Quebec, M
Lake Tanganyika, Africa, 0
Pacific Ocean, California Current
Fuller Pond, Connecticut, M
Sea of Japan, pelagic
Atlantic coastal fjord, Sweden
Sea of Japan
Lake Erken, Germany, M
Bay of Villefranche,
France
Char Lake, Canada (polar), 0
Long Island Sound, New York
Pacific coastal waters, California
Florida lakes, 0
Pacific Ocean, So. California Bight
Long Island Sound, New York
Black Creek, Georgia (blackwatcr)
Lake Magog, Quebec, E
Oslofjord, Sweden
King Lake, Ontario, 0
Venice Lagoon, Italy
Crosson Lake, Ontario, 0
Plastic Lake, Ontario, 0
De Castri Bay, Sea of Japan
Jack Lake, Ontario, 0
Ruth Lake, Ontario, 0
Three Milt Lake, Ontario, 0
Lake Waterloo, Quebec, E
Pacific Ocean, Peruvian upwelling
Pacific Ocean, coastal waters
Esthwaite Water, U.K., E
Florida lakes, M
Young Lake, Ontario, 0
Blue Chalk Lake, Ontario, 0
Mountain Lake, Ontario, 0
Antarctic Ocean (midsummer)
Pacific Ocean, equatorial upwelling
Kaneohe Bay, Hawaii
Rhode, Maryland (tidal river)
Reference
E
Bereczky 19 80
Baldock et al. 1983
Bigelow et al. 1940
Beers et al. 1982
Sorokin 198 1
Mamaeva 1976
Beers and Stewart 197 1
Pace 1986
Sorakin 198 1
Pace 1986
Pace 1986
Davis 1973
Pace 1986
Pace 1986
Taguchi 1976
Eriksson et al. 1977
Petrova et al. 1975
Pace 1986
Sorokin 198 1
Barn forth 195 8
Bownik-Dylinska
975
Pace 1986
Pace 1986
Hecky et al. 1978
Beers and Stewart 1967
Porter 1973~
Sorokin 198 1
Hedin 1975
Sorokin 1977
Nauwerck 1963
Rassoulzadegan and Gostan 1976
Rigler et al. 1974
Capriulo and Carpenter 1980
Beers and Stewart 1979
Beaver and Crisman 1982
Heinbokel and Beers 1979
Capriulo and Carpenter 198 3
This study
Pace 1986
Paasche and Ktistiansen 1982
Gates 1984
Sorokin 198 1
Gates 1984
Gates 1984
Sorokin 198 1
Taylor and Lean 198 1
Gates 1984
Gates 1984
Pace 1986
Sorokin 198 1
Beers et al. 1980
Bark 1981
Beaver and Crisman 1982
Gates 1984
Gates 1984
Gates 1984
Sorokin 198 1
Sorokin 198 1
Hirota and Szyper 1976
Berk et al. 1977
-
Protozoans
Table 4.
\
Cx 10’ liter-9
37.4
40
18-42
~0.02-46
55.5
86
~0.02-92
10-100
145
O-146
155.0
0.1-190
l-200
4.7-226
2-254
I .O-302
370
. 4-808
2,000-4,000
in blackwater
173
rivers
Continued.
Environment
Reference
and description
Gates 1984
Sorokin 198 1
Sorokin and Paveljeva 1972
Sanders 1987
Beaver and Crisman 1982
Sorokin 1981
Smetacek 198 1
Kume 1979
Sorokin 1981
This study
Beaver and Crisman 1982
Pace 1982
Pace and Orcutt 198 1
Sherr pers. comm.
Korniyenko
197 2
This study
Sorokin 198 1
Korniyenko
1972
Sorokin and Kogelschatz 1979
White Lake, Ontario, 0
Faro Lagoon, Sicily (meromictic)
Dalnee Lake, USSR, M
Damariscotta estuary
Florida lakes, E
Peruvian upwelling (diatom bloom)
Kiel Bight (estuary)
Tokyo Bay, Japan
Peruvian upwelling (“red tide”)
Ogeechec River, Georgia
Florida lakes, E
Lake Ogelthorpe, Georgia, E
Lake Ogelthorpe, Georgia, E
Duplin River, Georgia (estuary)
Lake Oktyabr’skoye,
M
Black Creek, Georgia (backwater)
Valpisani Pond, Italy (brackish)
Lake Karasum, USSR, E
Punta San Juan (“red water” bloom)
refractory material. In the Ogeechee the
vascular plant seston accounts for only 2.6%
of the total seston, however, while the AM
fraction is 83% (Wallace et al. 1987).
Because of the high microbial biomass,
the nitrogen content of AM can be great and
the nutritive value high. Scraper-grazer insects assimilated a polysaccaride matrix secreted by bacteria on stream rock surfaces
with 62-74% efficiency (Rounick and Winterbourn 1983). Although the densities of
protozoans in this organic layer were not
reported, it would seem to be an excellent
habitat for them. The only estimates available of the efficiency of assimilation of protozoans are by the predaceous oligochaete
Chaetogaster langi fed Vorticelia convallaria (assimilation
efficiency, 48%: Taylor
1980) and Daphnia magna fed two species
of ciliates (assimilation
efficiency, 6 5%:
Porter et al. 1979). If the microbial fraction
is 42% of AM in the Ogeechee River and
animals assimilate the microbial fraction
with a 50% efficiency, then the assimilation
of AM is at least 2 l%, even without assimilation of any of the other fractions. Estimates of assimilation
and importance of
amorphous material (bacteria, protozoans,
etc.) to filter-feeding macroinvertebrates
in
the Ogeechcc River would be greatly underestimated with the 5% assimilation efficiency usually applied to detritus (Benke and
Wallace 1980).
loo0
A
A
b)
1
pg chlorophyll
10
_a per liter
Fig. 5. The annual average Chl a and ciliate (a)
density and (b) biomass of the Ogeechee River (D)
compared with Ontario lakes (0) (Gates 1984), Quebec
lakes (0) (Pace 1986), and Florida lakes (A) (Beaver
and Crisman 1982). The regression equations are (a) y
= 8240x0.5’s and (b) y = ~O.~XO.~*‘. These regressions
do not include the Ogeechee River point. (Figure from
Porter et al. 1985; other data from M. Pace; Ogecchee
River annual Chl a from Edwards 1985.)
174
Carlough
and Meyer
Table 5. Literature values of the population densities of natural flagellate assemblages. Values are ranked
from lowest to highest based on the maximal reported density.
( x 1O6 liter- ‘)
0.00 1-O. 1
0.4
0.5
0.54
0.2-0.6
0.7
0.7
1.0
0.7-1.2
0.7-1.5
1.8
2.0
1.8-2.1
0.3-2.2
3.0
1.6-3.3
4.0
4.0
4.3
4.8
5.5
5.8
6.0
6.4
0.7-6.4
1.9-6.7
6.8
9.0
0.5-9.5
O-10
0.05-I 1
0.06-I 1
13.0
23
270
Environment
and descriplion
Esthwaite Water, U.K. (eutrophic lake)
Pacific Ocean, equatorial upwelling
Pacific Ocean, equatorial divergence
River Frome, U.K. (chalk stream)
N. Pacific Gyre
Black Sea, 130 m deep
Peruvian upwelling, frontal zone
Sargasso Sea, 20-m depth
Sargasso Sea, surface water
Western Sargasso Sea
Black Sea, pelagic
De Castri Bay, Sea of Japan
Upper Duplin River estuary
Atlantic Ocean, nearshore shelf
Pacific Ocean, Tradewinds area
Lower Duplin River estuary
Black Sea, coastal area
Venice Lagoon, Italy
Buzzards Bay, coastal Massachusetts
Valpisani Pond, Italy (brackish pond)
Woods Hole Harbor, coastal Massachusetts
Eel Pond, coastal Massachusetts
Peruvian upwelling (late diatom bloom)
Continental shelf edge, Massachusetts
Black Creek, Georgia (backwater)
Lake Oglethorpe, Georgia (eutrophic lake)
Vineyard Sound, coastal Massachusetts
Strong Peruvian upwelling
Sea of Japan, pelagic
Oregrundsgrcpen, Baltic Sea estuary
Black Creek, Georgia
Ogeechee River, Georgia
Peruvian upwelling (“red tide”)
Faro Lagoon, Sicily (meromictic)
“Red water” bloom
The role of the microbial loop in aquatic
food chains is slowly being unraveled. Although mechanisms of some microbial interactions are known, their importance to
the food web in lotic environments has rarely been addressed. Protozoans in the Ogeechec River are potentially important in controlling bacterial production and are a source
of carbon for filter feeders. Protozoans in
this river appear to play a role not only in
recycling nutrients, but also as food for
higher trophic levels.
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N
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N
N
Y
N
Y
Y
N
Y
Y
Y
Y
N
N
Y
Y
Y
N
N
Y
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Submitted: 28 May 1987
Accepted: 21 June I988
Revised: 3 November 1988