Journal of Plankton Research Vol.22 no.8 pp.1559–1577, 2000
Zooplankton grazing on bacteria and phytoplankton in a regulated
large river (Nakdong River, Korea)
Hyun-Woo Kim1,3, Soon-Jin Hwang2 and Gea-Jae Joo1
1Department of Biology, Pusan National University, Pusan, 609-735 and
2Department of Agricultural Engineering, College of Agriculture and Life
Sciences, Konkuk University, Seoul, 143-701, South Korea
3Present
address: Institute of Freshwater Ecology and Inland Fisheries,
Department of Shallow Lakes and Lowland Rivers, Müggelseedamm 301,
D-12562 Berlin, Germany
Abstract. Zooplankton grazing on bacteria and phytoplankton was evaluated at monthly intervals,
from March 1998 to March 1999, in the lower Nakdong River, Korea. We quantified bacterial and
phytoplankton carbon contents, and measured carbon ingestion rates (CIRs) by two size classes of
zooplankton: (i) microzooplankton (MICZ), ranging in size from 35 to 157 µm and including rotifers
and nauplii, but protists were excluded; and (ii) macrozooplankton (MACZ), of a size larger than 157
µm and including cladocerans and copepods. Two types of laboratory grazing experiments were
carried out to quantify zooplankton grazing on bacteria and phytoplankton. Species-specific and
community filtering rates were measured in the feeding experiments with representative fluorescent
microspheres (FM): 0.75 µm FM for bacteria and 10 µm FM for phytoplankton. CIRs were measured
using natural bacterial and phytoplankton communities in the zooplankton density manipulation
experiments. Bacterial carbon was considerably lower (average ± SD: 36 ± 24 µg C l–1, n = 25) than
phytoplankton carbon (383 ± 274 µg C l–1, n = 25). Total zooplankton carbon (236 ± 520 µg C l–1) was
usually dominated (>65%) by the MICZ fraction. Rotifers were the dominant taxonomic group.
Bacterial carbon was positively related to both MICZ and MACZ carbon (P < 0.05) seasonally, but
phytoplankton carbon was not. The community filtering rates (CFRs; ml l–1 day–1) and biomass
grazing rate (G; % day–1) of MICZ, on both bacteria and phytoplankton, were always higher than
those measured for MACZ. MICZ CIRs on bacteria (average 5.3 ± 5.5 µg C l–1 day–1) and phytoplankton (<35 µm in size) (average 63 ± 28 µg C l–1 day–1) were ~twofold higher than MACZ CIRs.
On average, MICZ accounted for 70 and 83% of total zooplankton grazing on bacteria and phytoplankton, respectively. Considering the total zooplankton community, MICZ generally were more
important than MACZ as grazers of bacteria and phytoplankton. Rotifers, in particular, played an
important role in transferring both bacterial and phytoplankton carbon to higher trophic levels in the
lower Nakdong River ecosystem.
Introduction
The important role of microbial-based pathways in plankton carbon dynamics
was first recognized by Gliwicz (Gliwicz, 1969), and in the last two decades it has
been an extensively studied topic. The ‘microbial loop’ has been documented in
a number of different limnetic ecosystems, including highly eutrophic bays and
mesotrophic Great Lakes (Hwang and Heath, 1997a,b, 1999). The concept of the
microbial loop is that bacterial production can be comparable to primary production, and that the bacteria are consumed by micro- and macrozooplankton.
Recently, several authors [e.g. (Sanders et al., 1989; Vaque and Pace, 1992; OomsWilms et al., 1995)] also concluded that bacterial standing crop can be suppressed
by zooplankton grazing, i.e. that the microbial loop can experience top-down
control, as occurs in the grazing food chain.
Although zooplankton grazing on phytoplankton (Thompson et al., 1982;
© Oxford University Press 2000
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H.-W.Kim, S.-J.Hwang and G.-J.Joo
Gosselain et al., 1996) and bacteria (Urabe and Watanabe, 1991; Hart and Jarvis,
1993; Hwang and Heath, 1999) have received increasing attention in freshwater
ecosystems, studies have mainly focused on the dynamics of particular taxa,
rather than whole communities. Moreover, the relative importance of bacteria
versus phytoplankton as food resources for zooplankton has seldom been
assessed in the rivers. Bacterioplankton have largely been excluded from models
of trophic interactions in river ecosystems.
Owing to the limited number of studies (Sellner et al., 1993; Gosselain et al., 1996;
Kobayashi et al., 1996), the question remains as to whether bacteria and phytoplankton are ‘links or sinks’ for carbon flow to higher trophic levels in rivers. In
other words, it is unknown whether a significant fraction of bacterial and phytoplankton carbon is utilized in the microbial loop and returned to the traditional
food web. In this study, we compared microzooplankton (MICZ; mostly nauplii and
rotifers, but protists were excluded) and macrozooplankton (MACZ; cladocerans
and copepods) grazing on bacteria and phytoplankton in a hypertrophic river
system, in order to provide information regarding plankton carbon dynamics.
Study site
The study site (~35°44N and 128°59E) is located at Mulgum, ~26.5 km upstream
of the mouth of the Nakdong River (the length of the main river channel = 528 km;
total catchment area = 23 817 km2) (Figure 1). Since the construction of the
Nakdong estuary dam in 1987, the study site has comprised freshwater, with a mean
depth of 3–4 m. The width of the river at this location is 250–300 m.
The middle to lower stretch of the Nakdong River is almost completely devoid
of littoral habitats (>90% sand substrata) and its course is homogeneous. Flow in
the upper river is irregular and is controlled by four dams on tributaries and on
the main river channel. Water flow in the lower river is more regular, due to the
estuary dam. The lower part of the river has become a ‘river–reservoir hybrid’
due to these changes in hydrology (Kim et al., 1998). Because the river has relatively high nutrient concentrations, it experiences blooms of cyanobacteria (e.g.
Microcystis aeruginosa) that are indicative of cultural eutrophication (Ha et al.,
1998, 1999).
Method
Sample collection and measurement of basic limnological variables
Sampling was conducted at bi-weekly intervals, from March 1998 to March 1999,
at the Mulgum location (Figure 1). Water samples were collected at 0.5 m depth
using a 3·2 Van Dorn bottle, placed in sterile 20 l polyethylene bottles, and kept
in the shade at ambient temperatures until return to the laboratory (within 1 h of
collection). Water temperature was measured using a YSI Model 58 thermistor.
Transparencies were determined using a 20 cm diameter Secchi disk, and pH was
measured using an Orion Model 407A meter. Dissolved oxygen was measured
using a YSI Model 58 meter, with calibration by Winkler titration (American
Public Health Association, 1995).
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Zooplankton grazing in Nakdong River, Korea
Fig. 1. Map showing the study site (•: Mulgum, river kilometer 26.5RK from the mouth of the river).
Bacterial enumeration and biomass determination
Bacterial samples were fixed with 5% cold glutaraldehyde solution (final concentration 1%), and cell abundances were determined on triplicate 50 ml samples of
river water. One milliliter of each sample was diluted with 0.2 µm-pre-filtered
distilled water to 1:10 or 1:20, and a 5 ml subsample of the resulting solution was
filtered on a black 0.2 µm GTBP Millipore membrane filter. Bacteria on the filters
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H.-W.Kim, S.-J.Hwang and G.-J.Joo
were stained with 4,6-diamidino-2-phenylindole (Porter and Feig, 1980). At least
300 cells were counted at 1000 magnification using a Zeiss epifluorescent microscope to calculate bacterial abundances. Mean cell volumes (µm3 cell–1) in each
sample were estimated from measurements of 100 random cells (Wetzel and
Likens, 1991). Bacterial carbon was estimated using a conversion factor of 2.2 10–13 g C µm–3 (Bratbak and Dundas, 1984).
Phytoplankton enumeration and biomass determination
After collection, phytoplankton samples were immediately preserved with
Lugol’s solution. Utermöhl’s sedimentation method was used to identify and
enumerate phytoplankton taxa in the samples (Utermöhl, 1958). Cells were
enumerated with a Zeiss IM inverted microscope at 400 magnification; a
minimum of 25 fields of view were counted per sample.
Phytoplankton carbon was calculated from measured biovolumes and
published cellular carbon contents. For each species, 10 individuals were
measured, and volumes (µm3 cell–1) were determined by approximating cell
shapes to regular geometric solids (Wetzel and Likens, 1991). Cellular carbon
content (µg C cell–1) was estimated by a conversion factor of 0.2 pg C µm–3 for
preserved non-diatom algal species (Strathmann, 1967). For diatoms, the following regression equation was used:
log C = –0.422 + 0.758 log V
where C is picograms of carbon and V is volume (µm3).
Zooplankton enumeration and biomass determination
Zooplankton were collected from 0.5 m depth using a 3.2 l Van Dorn bottle until
a total of 8 l of water was obtained. This water was filtered through a 35 µm mesh
net, and the retained zooplankton were preserved with 10% formalin (final
concentration). The zooplankton were divided into two size groups, with a 157
µm net, to count efficiently. Zooplankton >157 µm (almost exclusively copepods
and cladocerans) were counted with an inverted microscope at 25–50 magnification. Zooplankton <157 µm (mostly nauplii and rotifers) were counted with an
inverted microscope at 100–400 magnification. Zooplankton taxa were identified to genus or species (except for juvenile copepods) using as references Koste
(Koste, 1978), Smirnov and Timms (Smirnov and Timms, 1983), Koste and Shiel
(Koste and Shiel, 1987) and Bayly (Bayly, 1992).
Zooplankton biomass was estimated from published length–dry weight
relationships (Bottrell et al., 1976; Bird and Prairie, 1985; Culver et al., 1985).
Lengths were determined for >25 individuals of each crustacean taxon. Dry
weights of rotifers (except bdelloids) were obtained from the literature (Dumont
et al., 1975; Bottrell et al., 1976; Makarewicz and Likens, 1979). Dry weights of
bdelloids were estimated from their volumes, as was done with phytoplankton.
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Zooplankton grazing in Nakdong River, Korea
Carbon contents were calculated using a conversion factor of 0.48 µg C per µg
dry weight (Anderson and Hessen, 1991).
Laboratory grazing experiments and quantification of carbon ingestion
rates
Grazing experiments were conducted on 25 occasions from March 1998 to March
1999. Water samples in 2 and 4 l sterile polyethylene carboys were spiked with
0.75 or 10.0 µm fluorescent microspheres (FM), in amounts representing from 7
to 10% of natural bacterial and phytoplankton densities, respectively. To determine appropriate incubation periods, time course measurements (0, 2, 5, 10, 20
and 30 min) with both sizes of FM were made. Incubations lasted for 10–30 min,
after which the water was filtered through a 35 µm plankton net. The numbers of
fluorescent spheres in the guts of zooplankton grazers were counted and averaged for at least 5–20 individuals of each taxon. Species-specific filtering rates
(SFRs; ml animal–1 day–1) were calculated with the equation:
SFR = (St – S0)/M (T/1440 (min))
where St is the mean number of FM ingested per zooplankton species at incubation time t, S0 is the mean number of FM ingested per zooplankton species at
incubation time 0, M is the total concentration of FM added to carboys (no. ml–1)
and T is incubation time (min).
Community filtering rates (CFRs; ml l–1 day–1) of MICZ and MACZ were
determined as the sum of SFR for all representative taxa observed. Grazing rates
(G; % day–1) were determined as the percentage of the water volume filtered by
the whole zooplankton in the carboys.
Carbon ingestion rates (CIRs; µg C l–1 day–1) on bacteria and phytoplankton
were quantified experimentally by manipulating grazer zooplankton densities.
MICZ treatments were established by filling 2 and 4 l carboys with river water
and subsequently inoculating 35–157 µm zooplankton at densities of 1, 4, 8
and/or 16 ambient levels. MACZ treatments were established by filling 2 l
carboys with 35 µm-screened river water and subsequently inoculating zooplankton >157 µm at densities of 1, 4, 8 and/or 16 ambient levels. In each case,
there were also controls with no zooplankton added. All MICZ and MACZ treatments were duplicated during the study, except for two experiments in March and
April 1998. The river nutrient concentrations were very high during the study
period (phosphate: 117 ± 193 µg l–1; ammonia: 0.67 ± 0.97 mg l–1, n = 45), so that
we doubt that the nutrient recycling by zooplankton grazing seriously affected
the phytoplankton growth in the carboys. This fact is supported by nutrient limitation bioassay carried out at the same study site (March and April 1998;
Kim,H.W., Hwang,S.-J. and Joo,G.J., unpublished data).
All carboys were incubated for 24 or 48 h under ambient light and temperature conditions. Initial and final duplicate subsamples (25 ml) of bacteria and
phytoplankton were removed from the carboys, preserved, and enumerated as
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H.-W.Kim, S.-J.Hwang and G.-J.Joo
described above. Exponential growth rates were estimated using the following
equation:
r = (lnNt – lnNo)/t
where r is the rate of population growth (day–1), No and Nt are initial and final
cell densities (bacteria or phytoplankton), and t is the duration of incubation. The
relationship between phytoplankton and bacterial growth rate (dependent variable) and zooplankton biomass (independent variable) was assessed by leastsquares linear regression. The slope of this relationship provides an estimate of
the biomass-specific clearance rates (CRs; ml µg dw–1 day–1) of MICZ and
MACZ on phytoplankton and bacteria (Lehman and Sandgren, 1985). The CIRs
(µg C l–1 day–1) from phytoplankton and bacteria to MICZ and MACZ (µg C l–1
day–1) were calculated by the following equations:
PCIRs = CRs (phytoplankton biomass) (ambient MICZ or MACZ biomass)
BCIRs = CRs (bacterial biomass) (ambient MICZ or MACZ biomass)
where CRs are the MICZ or MACZ clearance rates on phytoplankton and
bacteria, respectively (ml µg dw–1 day–1), phytoplankton and bacterial biomass is
in µg C l–1, ambient zooplankton biomass is µg dw l–1, PCIRs are the phytoplankton carbon ingestion rates and BCIRs are the bacterial carbon ingestion
rates.
Statistical analysis
One-way analysis of variance (ANOVA) was used to compare environmental
parameters among months of sampling. A Student’s t-test was used to compare
zooplankton biomass and abundance between years. Pearson’s coefficients were
used to determine the correlations between certain biotic variables. Statistical
analyses were performed using SAS Stat Version 6.12 (Statistical Analysis
Systems Institute, 1996). Significant differences and correlations were identified
as P < 0.05.
Results
Basic limnology
During the study, water temperatures varied from 3 to 28°C (Figure 2a). During
spring (April–May) and winter (December–January), water temperatures were
highly variable. During summer, due to the frequent rain events, water temperature did not exceed 30°C. Low Secchi transparencies were generally observed
(average ± SD: 67 ± 23 cm, n = 25) (Figure 2b). However, in May and October,
Secchi depths were much greater (>100 cm), while the lowest Secchi depths
(<60 cm) occurred in summer. pH and dissolved oxygen (DO) gradually
increased during spring, fall and towards the end of winter of 1999 (Figure 2c).
1564
Zooplankton grazing in Nakdong River, Korea
Fig. 2. Changes in the basic limnological parameters (a) water temperature, (b) Secchi depth and (c)
pH and dissolved oxygen during the study period (March 1998–March 1999).
Average pH and dissolved oxygen (DO) concentration were 8.0 ± 0.9 and 10.9 ±
3.6 mg l–1 (n = 25) during the study period. During midsummer (July–August),
both pH (<7.0) and DO concentrations (<7.0 mg l–1) were low.
Seasonal changes of river bacteria and phytoplankton biomass
There were statistically significant seasonal differences in bacterial abundance
and biomass (ANOVA, P < 0.05). The patterns of seasonal variation in the two
attributes were similar. Large changes in bacterial abundance and biomass were
observed between May and November, while small changes occurred from
December to March (Figure 3a and b). Bacterial abundance and biomass varied
from 0.2 106 to 7.6 106 cells ml–1, and from 2.26 to 86.2 µg C l–1, respectively.
Mean abundance and biomass values were 3.1 ± 2.1 106 cells ml–1 and 36 ± 24
µg C l–1, respectively. Both abundance and biomass were highest in late June and
early September, and lowest in mid-August. Maximal values of bacterial biomass
coincided with the maximal values of phytoplankton biomass during the study
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H.-W.Kim, S.-J.Hwang and G.-J.Joo
Fig. 3. Seasonal changes in bacterial and phytoplankton biomass and abundance during the study
period (March 1998–March 1999).
(r = 0.583, P < 0.002, n = 25). However, there was not a significant relationship
between bacterial and phytoplankton abundance (r = 0.363, P > 0.1, n = 25).
Phytoplankton abundance differed significantly among seasons (ANOVA,
P < 0.05), while seasonal variation of biomass was not significant. During nine
months of 1998 (March–November), a low phytoplankton abundance (<1.0 104
cells ml–1) consistently occurred, with the exception of late June (2.5 104
cells ml–1) and late November (2.3 104 cells ml–1). Peaks in phytoplankton
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Zooplankton grazing in Nakdong River, Korea
abundance were also observed during December through March 1999 (Figure 3c).
At those times, the dominant phytoplankton taxa were diatoms. In particular,
Stephanodiscus hantzschii accounted for >80% of total phytoplankton abundance.
Phytoplankton biomass (average ± SD: 383 ± 274 µg C l–1, n = 25) was always
higher than bacterial biomass (36 ± 24 µg C l–1). The highest phytoplankton
biomass occurred in late June (1530 µg C l–1) (Figure 3d).
Micro- and macrozooplankton biomass and correlations
The seasonal variation in total zooplankton biomass was significant (ANOVA,
P < 0.01). Only on six occasions did total zooplankton biomass exceed the mean
value of 236 ± 520 µg C l–1, with the highest peak occurring in late May (2200
µg C l–1) (Figure 4a). The seasonal pattern of MICZ biomass was similar to that
of total zooplankton (Figure 4b). During heavy rainfall events and floods in
August, biomass decreased sharply. After the flooding ended, both MICZ and
Fig. 4. Seasonal changes in total zooplankton, microzooplankton (MICZ) and macrozooplankton
(MACZ) biomass.
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H.-W.Kim, S.-J.Hwang and G.-J.Joo
MACZ biomass increased rapidly and recovered to pre-flood levels within <1
month.
Total mean biomass of rotifers was significantly higher (P < 0.001, t-test, n = 25)
than observed for other zooplankton groups (rotifers = 120 ± 144 µg C l–1; cladocerans = 20 ± 66 µg C l–1; copepods = 40 ± 130 µg C l–1; nauplii = 10 ± 26 µg C l–1).
Among the MICZ, nauplii biomass was negligible except in mid-July, when
nauplii relative abundance was 63%. Average MACZ biomass (average ± SD:
83 ± 224 µg C l–1) was lower than MICZ biomass (153 ± 326 µg C l–1). In late
spring and early fall, high peaks (>100 µg C l–1) of MACZ biomass were observed
(Figure 4c). Among the MACZ, copepod biomass was twofold higher than cladoceran biomass. Both copepod and cladoceran biomass were maximal in June and
minimal in January.
Total zooplankton biomass was significantly correlated with bacterial biomass,
but not with the biomass of phytoplankton (Table I). Furthermore, both MICZ
and MACZ biomass were significantly correlated with bacterial biomass. Among
the MICZ and MACZ, rotifer and copepod biomass displayed significant
relationships with bacterial biomass. None of the major zooplankton taxonomic
(rotifers, cladocerans, nauplii and copepods) or size (MICZ and MACZ) classes
had significant biomass correlations with phytoplankton.
Species-specific and community filtering rates based on microsphere uptake
During laboratory grazing experiments, some zooplankton never had microspheres in their guts, while other zooplankton always took up the spheres (Table
II). The mean SFR (ml animal–1 day–1) for rotifers varied from 0.002 to 0.726, and
>90% of the individuals grazed both sizes of spheres (0.75 and 10 µm). The
highest SFR values were observed for Brachionus angularis, Brachionus calyciflorus and Filinia longiseta. For cladocerans and copepods, the mean SFR ranged
from 0.05 to 0.878 and from 0.041 to 0.3, respectively. All cladocerans except
Alona spp. grazed spheres. The highest SFR values were observed for Bosmina
longirostris (average ± SD: 0.878 ± 0.925). The average SFR for cyclopoids
feeding on 0.75 µm spheres was very low, never exceeding 0.05, while the average
SFR of cyclopoids feeding on 10 µm spheres was high (0.3 ml animal–1 day–1).
CFRs and grazing rates varied from 2 to 1670 ml l–1 day–1 and from 0.1 to 167%
day–1, respectively. The CFRs of MICZ were much higher than for MACZ
Table I. Pearson correlation coefficients between zooplankton biomass (µg C l–1) and bacterial and
phytoplankton biomass (µg C l–1) in the lower Nakdong River (March 1998–March 1999, n = 25)
Log10 biomass
Log10 biomass
––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––
RO
CL
CO
NA
MICZ
MACZ
TZ
Bacteria
Phytoplankton
0.401*
0.243
0.331
0.036
0.484*
0.190
0.117
–0.336
0.410*
0.169
0.469*
0.101
0.429*
0.150
RO, rotifers; CL, cladocerans; CO, copepods; NA, nauplii; MICZ, microzooplankton (rotifers and
nauplii); MACZ, macrozooplankton (cladocerans and copepods); TZ (total zooplankton).
Significant correlations: *P < 0.05.
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Table II. Species-specific filtering rate (SFR; ml animal–1 day–1) in the lower Nakdong River as
measured by uptake of microspheres
SFR
Bacteria size (0.75 µm)
Phytoplankton size (10 µm)
ROTIFERS
Anuraeopsis fissa
Asplanchna spp.
Brachionus angularis
B.calyciflorus
B.forticula
B.rubens
B.ureolaris
B.quadridentatus
Conochilus unicornis
Filinia longiseta
Hexarthra mira
Keratella cochlearis
K.valga
Lecane spp.
Lepadella oblongata
Monostyla spp.
Notholca labis
Philodina spp.
Polyarthra spp.
Synchaeta spp.
Trichocerca spp.
0.036 ± 0.027
0.110 ± 0.238
0.726 ± 0.285
0.039 ± 0.046
nf
0.172 ± 0.186
0.144 ± 0.138
0.017 ± 0.016
0.172 ± 0.074
0.653 ± 0.486
0.342 ± 0.318
0.009 ± 0.008
0.012 ± 0.017
0.007 ± 0.006
0.022 ± 0.030
0.007 ± 0.010
0.011 ± 0.016
0.085 ± 0.029
0.004 ± 0.004
0.003 ± 0.003
0.002 ± 0.001
nf
0.195 ± 0.203
0.043 ± 0.040
0.684 ± 1.012
0.037 ± 0.027
0.030 ± 0.019
0.116 ± 0.180
0.081 ± 0.064
nf
0.040 ± 0.042
0.215 ± 0.243
0.002 ± 0.002
0.002 ± 0.001
0.001 ± 0.001
0.002 ± 0.001
nf
0.145 ± 0.149
0.123 ± 0.090
0.127 ± 0.112
0.031 ± 0.019
0.009 ± 0.009
CLADOCERANS
Alona spp.
Bosmina longirostris
Bosminopsis deitersi
Diaphanosoma brachyurum
Moina micrura
nf
0.878 ± 0.925
0.062 ± 0.080
0.068 ± 0.074
0.267 ± 0.123
0.083 ± 0.017
0.167 ± 0.397
0.050 ± 0.049
0.374 ± 0.274
0.095 ± 0.107
COPEPODS
Cyclops copepodids
Nauplii
0.001 ± 0.002
0.003 ± 0.002
0.300 ± 0.353
0.111 ± 0.115
nf, not found.
(Figure 5a and b). The average CFRs of MICZ for bacteria and phytoplankton
were 50 ± 95 and 151 ± 262 ml l–1 day–1, respectively. The average CFRs of MACZ
for bacteria and phytoplankton were 20 ± 58 and 22 ± 65 ml l–1 day–1, respectively.
The highest CFRs for MICZ and MACZ were observed at different times. Total
zooplankton filtering rates on phytoplankton were much higher than filtering
rates on bacteria, especially late in the growing season (May, June and
November).
The trend in zooplankton grazing rates followed the changes in CFRs (Figure
5a and b). Relatively high grazing rates on bacteria and phytoplankton occurred
from May to June, and in November 1998. Total zooplankton grazing rates on
phytoplankton were higher than grazing rates on bacteria. However, in late
August, grazing rates on bacteria were slightly higher than on phytoplankton.
Based on bacterial-sized microsphere grazing, Brachionus angularis, B.rubens,
Conochilus unicornis, F.longiseta and Bosmina longirostris were the most
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Fig. 5. Changes in MICZ and MACZ community filtering rates (CFRs; ml l–1 day–1) on bacteria-size
(0.75 µm) and phytoplankton-size microspheres (10 µm) and grazing rate (G; % day–1).
important bacterivorous zooplankton. Brachionus calyciflorus, Notholca labis
and cyclopoid copepodids had high filtering rates on phytoplankton-sized microspheres (Figure 6). Seasonal variations were also observed. Among the species
that took up bacterial-sized microspheres, B.angularis (May–June and August),
B.rubens (May), C.unicornis (May–June and August), F.longirostris (May–June
and November) and B.longiseta (May–June) showed high filtering rates.
Brachionus calyciflorus (May–June and November–December), copepodids
(May–September) and N.labis (November through March of 1999) were the most
important species grazing on phytoplankton.
Biomass-specific clearance and carbon ingestion rates on natural bacteria
and phytoplankton
The range of biomass-specific CRs (ml µg dw–1 day–1) for MICZ and MACZ on
bacteria and phytoplankton varied from 0.03 to 10 and 0.01 to 10.1, and from 0.01
to 4.8 and 0.04 to 4.6, respectively (Table III). The average CR of MICZ on
bacteria (2.05 ± 2.77 ml µg dw–1 day–1) was nearly twofold higher than the average
CR of MACZ (1.23 ± 1.27 ml µg dw–1 day–1), while MICZ and MACZ CRs on
phytoplankton were approximately equal (MICZ: 2.33 ± 2.98 ml µg dw–1 day–1;
MACZ: 2.03 ± 1.65 ml µg dw–1 day–1). CRs differed significantly by season
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Fig. 6. Filtering rates of dominant zooplankton species (ml l–1 day–1) on bacteria and phytoplankton.
Filtering rates were measured by microsphere uptake experiments with 0.75 and 10 µm microspheres
for bacteria and phytoplankton, respectively (n = 25).
(ANOVA, P < 0.01). In spring and winter, CRs were higher than at other times,
except for the high CRs in July on phytoplankton (4.0 and 2.9 ml µg dw–1 day–1
for MICZ and MACZ, respectively) and in October on bacteria (4.2 and 1.2
ml µg dw–1 day–1).
Monthly variations of bacterial and phytoplankton CIRs (µg C l–1 day–1) to
MICZ and MACZ were significant (ANOVA, P < 0.05). BCIRs to total zooplankton (MICZ + MACZ) were lower than PCIRs. In spring and fall, BCIRs to MICZ
and MACZ were 10–15 times higher than during summer and winter (Figure 7a
and b). BCIRs to MICZ and MACZ ranged from 0.05 to 14.8 and from 0.01 to
7.1, respectively. Average BCIRs to MICZ were ~twofold higher than for MACZ
(MICZ: 5.3 ± 5.5; MACZ: 2.0 ± 2.4). PCIRs to MICZ were usually higher than to
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Table III. Biomass-specific clearance rates (ml µg dw–1 day–1) of zooplankton in the Nakdong River
Month
1998
March
April
May
June
July
August
September
October
November
December
1999
January
February
March
MICZ
–––––––––––––––––––––––––––––––
B
P
1.2
2.1
0.2
0.03
0.8
0.03
0.5
4.2
0.4
1.7
1.2
10.0
4.3
0.6
3.4
0.4
0.01
4.0
0.3
0.06
0.9
0.02
1.1
5.4
10.1
4.1
MACZ
––––––––––––––––––––––––––––––––––
B
P
0.7
1.5
0.4
0.3
0.1
0.01
0.3
1.2
1.3
1.5
1.3
3.7
0.9
0.04
2.9
1.0
0.6
0.5
3.9
0.1
1.6
4.8
2.3
4.6
3.2
3.7
B, river bacteria; P, river phytoplankton; MICZ, microzooplankton; MACZ, macrozooplankton.
MACZ (Figure 7c), but PCIRs to MACZ were higher than to MICZ in June,
August, September and November.
Discussion
In the lower Nakdong River, microzooplankton (MICZ: rotifers) play a more
important role in grazing bacteria and phytoplankton than do macrozooplankton
(MACZ: cladocerans and copepods). The most important MICZ grazers, on both
bacteria and phytoplankton, are rotifers. A similar result was observed at coastal
and offshore sites of Lake Erie, where rotifers were usually more important
bacterivores than cladocerans (Hwang and Heath, 1999). Rotifers have been
found to be the dominant grazers in other ecosystems, including freshwater estuaries in the USA (Havens, 1994), marine estuaries in Germany (Arndt and
Heerkloos, 1989) and small eutrophic lakes in France (Lair and Ali, 1990),
although sometimes this is not the case (Christoffersen et al., 1990).
Although there were not much data available, the importance of MICZ in
community grazing and plankton community structure shift was reported in some
river ecosystems. The mean grazing rate of MICZ on phytoplankton in River
Meuse was 19 ± 11% day–1 (n = 5) (Gosselain et al., 1996), which is similar to our
results (17 ± 31% day–1, n = 25). MICZ community grazing appears to constitute
an important process altering the phytoplankton community structure in the
Hawkesbury-Neapean River (Kobayashi et al., 1996). We also observed that the
small-sized phytoplankton community [greatest axial linear dimensions (GALD)
<20 µm, e.g. S.hantzschii] passed their peak stage in mid-spring, followed by the
dominance of colonial green algae and large diatoms (GALD >100 µm). In
the mid-spring experiments (Figure 5b), MICZ community filtering rates on
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Zooplankton grazing in Nakdong River, Korea
Fig. 7. Bacterial carbon ingestion rates (BCIRs) by MICZ and MACZ (a, b), and percent phytoplankton carbon ingestion rates (PCIRs) by MICZ and MACZ (c).
phytoplankton increased sharply from 200 to 1100 ml 1–1 day–1. Grazing by MICZ
in spring might be a main force to affect the decline of small phytoplankton
community abundance in the Nakdong River system.
In meso-eutrophic lakes, MACZ (mainly Daphnia) can impact nearly all of the
microbial components of the food web (Geetz-Hansen et al., 1987; Stockner and
Shortreed 1989; Pace et al., 1990). They have the ability to graze bacteria at rates
sufficient to remove most or all of the daily production (Kankaala, 1988).
However, at the two extremes of the nutrient gradient in lakes (ultra-oligotrophic
to hypereutrophic), where small copepods and cladocerans are predominant,
most components of the microbial food web are thought to remain intact and
largely unaffected by grazing (Nagata and Okamoto, 1988; Christoffersen et al.,
1990). We observed that Bosmina Longirostris (a small-bodied species) was a
dominant grazer of bacteria in the Nakdong River, but it did not appear to graze
at a rate that would significantly control the bacterial community. A similar result
was found in Dutch lakes, where B.longirostris and B.coregoni were the most
important grazers (Gulati et al., 1991).
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H.-W.Kim, S.-J.Hwang and G.-J.Joo
Our results also confirm that grazing by copepods does not seriously impact
bacteria, although their grazing may influence the phytoplankton. As we
observed in this river, copepod bacterivory at very low rates has been demonstrated in other environments (Pedros-Alio and Brock, 1983; Forsyth and James,
1984). Generally, copepods can influence the standing stocks of heterotrophic
nanoflagellates and small ciliates (Stoecker and Capuzzo, 1990; Gifford, 1991;
Wylie and Currie, 1991; Burns and Gilbert, 1993). Therefore, ‘indirect’
bacterivory, i.e. copepod grazing on protists that have consumed bacteria, may be
significant (Burns and Schallenberg, 1996; Hwang and Heath, 1997a).
The filtering rate by total zooplankton on phytoplankton was slightly higher
than on bacteria in this study. We conclude that phytoplankton are relatively
more important as a food source for the total zooplankton community in the
lower Nakdong River. Christoffersen et al. reported that total zooplankton had
high ingestion rates on phytoplankton, but low ingestion rates on bacteria during
in situ grazing experiments (Christoffersen et al., 1990). The results are similar to
those of our study. The efficiency of grazing on the small-sized fraction (bacteria)
was 2–4 times lower than for larger particles (phytoplankton). In summer, the
Nakdong River generally contains an abundance of cyanobacteria (Ha et al.,
1998, 1999). Because colonial cyanobacteria are considered to be an inadequate
food source of zooplankton (Lampert, 1985), the role of bacterivorous zooplankton during this season could be potentially important.
Zooplankton grazing activities in the Nakdong River are within the range
found in the literature for lakes. Rothhaupt reported that the SFR of B.calyciflorus was near 0.72 ml day–1 (Rothhaupt, 1990b). The SFR increased with particle size and was highest for particles of 10 µm diameter (Rothhaupt, 1990a). A
similar result was found in this study. Bogdan and Gilbert found SFR values
between 0.024 and 1.272 ml day–1 for Keratella spp. (Bogdan and Gilbert, 1982).
For other species, the literature reports values of 0.001–0.336 ml day–1 for
Synchaeta (Bogdan et al., 1980; Gilbert and Bogdan, 1984), 0.008–0.05 ml day–1
for Polyarthra spp. (Bogdan et al., 1980), 0.042–0.096 ml day–1 for B.angularis
(Walz, 1983; Rothhaupt, 1990a) and 0.072–0.264 ml day–1 for B.rubens (Rothhaupt, 1990a). The large variability, even within the same species, may depend
on some ecological conditions (e.g. temperature, food quantity and quality,
competition with other zooplankton, etc.). When zooplankton were fed fluorescent microspheres in our study, some cladocerans (e.g. Bosmina and Moina)
had a two- to 10-fold greater SFR than rotifers, but some rotifers (e.g. B.angularis and Filinia) had a greater SFR than small cladocerans. Even though the
grazing activity of zooplankton (SFR) and grazing rates (G) of food sources
differed, the MICZ appeared to be important bacterial and phytoplankton
grazers in this study.
In studies of the plankton food web of Lake Erie, USA, Hwang and Heath
concluded that MICZ were important bacterial grazers, and that bacteria were
an important source of carbon for the food web (Hwang and Heath, 1999). In our
study, evidence of an active grazing relationship between bacteria and MICZ, and
between bacteria and MACZ, indicates that zooplankton (mostly rotifers)
actively graze bacteria in the lower Nakdong River, and that bacteria may be an
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Zooplankton grazing in Nakdong River, Korea
important carbon source for higher trophic levels in river ecosystems. However,
we recognize that the study site was hypertrophic and that the role of the microbial loop may vary with different trophic status (mesotrophic–hypertrophic) and
with dominant taxa among the zooplankton community in the middle and upper
part of the river, as it does in lakes (Pace et al., 1990; Weisse et al., 1990; Wylie
and Currie, 1991; Hwang and Health, 1997b). Further research is needed to determine the degree to which our results can be generalized.
Although our data did not demonstrate protist grazing on bacteria and detritus, lotic protists can consume bacterial biomass as rapidly as protists in marine
and lentic ecosystems (Hwang and Heath, 1997a). Further information about the
number of trophic transfers within the microbial loop and the efficiency of carbon
transfer between each level is needed to define the overall role of protists in the
food web in the Nakdong River and in other river ecosystems.
Acknowledgements
The authors greatly acknowledge the comments of three anonymous referees,
which improved the earlier version of this manuscript. This study was supported
by Korean Research Foundation (KRF) (project no. 1-D-00405) and a Young
Scientist Award from KRF to H.W.K. (1998).
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Received on August 5, 1999; accepted on March 10, 2000
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