Download Relative impacts of copepods, cladocerans and

Journal of Plankton Research Vol.18 no.5 pp.683-714.19%
Relative impacts of copepods, cladocerans and nutrients on the
microbial food web of a mesotrophic lake
Carolyn W.Burns and Marc Schallenberg
Department of Zoology, University ofOtago, PO Box 56, Dunedin, New
Zealand
Abstract. Calaneid copepods, rather than cladocerans, frequently dominate the zooplankton of lakes
in New Zealand. The potential consequences of this domination for the microbial community of mesotrophic Lake Mahinerangi, New Zealand, were determined by field experiments in which Boeckella
and Daphnia were added to in situ enclosures in the presence and absence of added nutrients. Boeckella
hamata at ambient densities (2 and 81~') rapidly and severely suppressed ciliate population growth over
4 days, even when microbial growth was enhanced by added nutrients, but effects of copepods on other
components of the microbial community (bacteria, photosynthetic picoplankton, heterotrophic nanoflagellates, algae) were slight. In contrast, Daphnia carmata at the same densities (but 3-fold higher
biomasses per litre) had a relatively weak effect on ciliates, suppressing ciliate abundance only after 4
days at 8 Daphnia I 1 (330 ^.g I 1 ); this daphniid density also depressed abundances of large bacterial
rods, some photosynthetic picoplankton and the dominant alga, Cyclotella. These results highlight the
relative importance of specific trophic linkages in a microbial food web; they also suggest that the
dominance of Boeckella in many southern hemisphere lakes may account for relatively low ciliate
abundances in these lakes.
Introduction
There have been numerous studies of the effects of nutrients (bottom-up) and
predation (top-down) in regulating the biomass and productivity of phytoplankton and zooplankton in lakes (references in DeMelo et al., 1992); far less is
known about how nutrients and consumers may interact to regulate planktonic
microbial communities (ciliates, flagellates, picoplankton, bacteria). In nutrientlimited systems, consumers may influence microbial diversity and biomass directly
by 'predation', and indirectly by the excretory release of nutrients. Several studies
in northern hemisphere lakes have related decreases in biomass and growth rates
of microbial organisms to increases in the biomass of zooplankton, particularly
Daphnia (reviewed by Jtlrgens, 1994). These Daphnia-based studies form the basis
of most current models of planktonic microbial food webs and grazer-mediated
effects (Riemann and Christoffersen, 1993; Jiirgens, 1994).
Calanoid copepods dominate the zooplankton biomass of the sea and are
important components of the zooplankton of lakes, particularly in temperate
latitudes. Comparatively little is known, however, about the effects of calanoid
copepods on the microbial communities of lakes. Species of Diaptomus have the
potential to suppress the growth of ciliates (Burns and Gilbert, 1993; Hartmann et
al., 1993; Brett et al., 1994; Wiackowski et al., 1994) at least as effectively as a comparable biomass of Daphnia (Wiackowski etal., 1994). Thus, predation on ciliates
by copepods is a potentially important link between the organisms that comprise
the 'microbial loop' (Azam et al., 1983) and the classical food chain (nutrientsphytoplankton-zooplankton-fish) (Stoecker and Capuzzo, 1990; Pace and Funke,
1991; Burns and Gilbert, 1993; Wiackowski et al., 1994). Studies in Castle Lake,
California, have compared the effectiveness of Daphnia, Holopedium, Diaptomus
© Oxford University Press
683
C.W.Burns and M.Schallenberg
and Diacyclops in altering algal and bacterial biomass, and in depressing ciliate
growth rates, and hence in altering ciliate community structure (Brett et al., 1994;
Wiackowski et al., 1994), but indirect effects of calanoid copepods on other heterotrophs have not been measured. Jiirgens et al. (1994a) described the effects of
Daphnia spp. and mixed copepods (Eudiaptomus and three species of cyclopoids)
on the largely heterotrophic, microbial community of a mesotrophic lake, but the
relative effects of Daphnia and calanoids on net growth rates of autotrophic and
heterotrophic components of microbial food webs have not been determined.
Suspension-feeding calanoid copepods of the genus Boeckella dominate the
zooplankton of many lakes in New Zealand throughout the year. Daphnia are
absent or rare in many lakes, and common only briefly in a few mesotrophic and
eutrophic lakes; predation pressure on mesozooplankton appears to be low as
there are few invertebrate predators and no obligate planktivores (Chapman and
Green, 1987). Thus, the crustacean zooplankton may be the 'top predators' in the
pelagic zone of many New Zealand lakes for considerable periods of the year.
One way of gaining insight into the relative importance of top-down and
bottom-up regulation of populations and biomass in natural communities is by
manipulating resources and consumers. Many studies of microbial communities in
lakes have focused on only one or two components of the microbial loop; comparatively few have incorporated all of the major components, including nutrients and
algae (exceptions include Christoffersen etal., 1990; Arndt and Nixdorf, 1991; Pace
and Funke, 1991; Brett et al., 1994; Jurgens et al., 1994b). Pace and Funke (1991)
used the manipulative approach in a study of the effects of nutrients and Daphnia
on the heterotrophic microbes of two Michigan lakes, but effects of copepods were
not examined; Jiirgens et al. (1994a) did not distinguish between calanoids and
cyclopoids in their study of the effects of macrozooplankton on the bacterial community. The study by Brett et al. (1994) is the only one to compare the effects of
Daphnia and a calanoid, Diaptomus, on natural microbial communities of a lake.
In order to derive general predictions for the effects of cladocerans and copepods
on the trophic dynamics of lakes, more studies on the relative impacts of cladocerans and copepods are needed. In our study, we use an experimental approach
similar to that of Pace and Funke (1991) in which we manipulate nutrients and
consumers in in situ enclosures to determine (i) the relative impacts of Daphnia
and Boeckella on the microbial community of a mesotrophic lake, and (ii) the relative importance of top-down and bottom-up effects on algal biomass and the major
components of the microbial community in summer.
Study site and method
Lake Mahinerangi (surface area 18.6 km2, mean depth of 6.2 m) is a mesotrophic,
polymictic, reservoir. Daphnia carinata King and Boeckella hamata Brehm dominate the zooplankton biomass, reaching maximum densities of 6 and 9 1"' (adults
and CV instars), respectively (Burns, 1992).
This study was carried out from 6 to 10 December 1993 at a time when Lake
Mahinerangi was isothermal at 13°C and well oxygenated, the chlorophyll a concentration was 3.1 p.g I"1 and the Secchi depth was 1.05 m. Suspended clay
684
Microbial food web of a mesotrophk lake
[~2 mg I"1 ash-free dry weight (wt)] and colour (absorbance at 440 nm ~1.5 nr1)
contribute to the consistently low transparency of the lake. Average zooplankton
densities in the water column at the time were: adult Boeckella 2.25 I 1 (total copepodites 6.5 I 1 ), adult Daphnia 2 I"1 (total Daphnia 3.75 I"1) Bosmina 7.5 I"1, Ceriodaphnia dubia 12.2 I"1, Synchaeta (250 jim) 23 I"1 and Keratella 47 I"1. Water
collected from 2 m depth with Van Dorn bottles was screened through 150 jjim
mesh to remove large zooplankton and mixed in three large, covered barrels.
Thirty, 4.25 1 polyethylene enclosures (Cubitainers) were filled with well-mixed
water, after which nutrients and zooplankton were added in a combined factorial
and gradient design (Table I). Nutrients (NH4C1 and KH2PO4), to give added concentrations of 120 ng nitrogen (N) I"1 and 10 jig phosphorus (P) I"1, were added to
half of the enclosures. At the time of sampling, the inorganic nutrient concentrations in Lake Mahinerangi were 62 (xg I"1 N and 1.2 jo-g 1-' soluble reactive phosphorus (SRP) with a ratio of total nitrogen to total phosphorus (TN:TP) of 12:1.
Zooplankton for addition to the enclosures were collected in the lake on the previous day by vertical hauls from 5 m, sorted to species and kept in filtered lakewater in the dark at 13°C. Egg-bearing D.carinata (body length 1.87 ± 0.012 mm SE)
or B.hamata (prosomal length 1.06 ± 0.005 mm SE) were added at approximately
ambient densities (2 I"1) and four times ambient; six enclosures contained no added
crustaceans (Table I). Enclosures were assigned randomly to one of eight
anchored buoys from which they were resuspended in the lake at a depth of 1 m
below the surface for 4 days. Samples of the water that was used to fill the enclosures were collected for analysis of chlorophyll a, nutrients and microorganisms
(see below).
Enclosures were sampled after 1 day when grazing effects (top-down) of crustaceans were expected to dominate because 24 h is too short for most microorganisms to multiply significantly in response to nutrients (e.g. Carrick et al.,
1991), and after 4 days to allow the microbial community to respond to the combined effects of grazing and nutrient recycling (top-down and bottom-up effects)
while minimizing enclosure effects (sedimentation, growth on enclosure walls)
(e.g. Elser and Goldman, 1991; Pace and Funke, 1991). When the enclosures were
sampled after 1 day, the water that was removed (8% of total volume) was replaced
with freshly collected, 150 u,m-filtered lake water collected from 2 m and the nutrient-enriched enclosures received a second dose of nutrients at the same levels as
the initial dose. The enclosures were resuspended at the incubation depth for a
further 3 days.
Table I. Treatments of enclosures and abbreviations for treatments. All treatments were replicated
three times
Low nutrients
(no added nutrients)
High nutrients
(added nutrients)
OL
2DL
8DL
2BL
8BL
OH
2DH
8DH
2BH
8BH
No Daphnia or Boeckella
Daphnia 2 I"1
Daphnia 8 H
Boeckella 2 1 1
Boeckella 8 H
No Daphnia or Boeckella
Daphnia 2 I"1
Daphnia 8 I 1
Boeckella 2 1'
Boeckella 8 1'
685
C.W.Burns and M^diailenberg
When the enclosures were retrieved on day 4, they were subsampled again for
microorganisms, after which the entire contents of each enclosure were filtered
through 150 n.m mesh to retrieve the zooplankton for biomass determinations;
samples of the filtrate were taken for analysis of inorganic nutrients and chlorophyll a. Zooplankton were rinsed in distilled water, sorted under a dissecting
microscope to remove any debris and decaying animals, dried at 50°C for 48 h and
weighed on a Sartorius microbalance. All living zooplankton that were retrieved
from an enclosure contributed to the total biomass for that enclosure. Chlorophyll
a was measured spectrophotometrically (Shimadzu Model UV-120-01) on
acetone-extracted samples (0.5 1) that had been collected on GF/F filters (Pridmore el al., 1983). P and N concentrations were determined spectrophotometrically using a Chemlab autoanalyser according to standard procedures (Wetzel and
Likens, 1991); SRP was analysed using the antimony-ascorbate-molybdate
method, NH4-N was measured by the phenol-hypochlorite method, NCyN was
measured after reduction to NO2-N in a cadmium-copper column and TN and TP
were measured after oxidation in the presence of boric acid and sodium hydroxide
(Valderra, 1981). Samples of 300 ml for ciliates, small rotifers (<150 (xm) and algae
were preserved with 1% Lugol's iodine, concentrated by sedimentation and
counted at x300 magnification under an inverted light microscope. Samples for
picophytoplankton (5 ml) andflagellates(15 ml) werefixedwith equal volumes of
ice-cold 4% glutaraldehyde and collected on black polycarbonate 0.8 (im (flagellates) and 0.2 |im (picoplankton)filtersbefore staining with primulin (Bloem et al.,
1986). Samples for bacteria were fixed with 0.5% formalin and frozen until
analysis. Subsamples (1.5 ml) of the thawed samples were collected on black
0.2 \im filters, stained with DAPI (Porter and Feig, 1980) and counted immediately using fluorescence microscopy. Counts were made at xlOOO magnification
under a Zeiss Axiophot microscope equipped with filter sets for UV excitation
(BP365/11/FT395/LP397) for heterotrophic flagellates and bacteria, and green
excitation (BP546/12/FT580/LP590) for picophytoplankton and photosynthetic
flagellates. As so few picoplankton cellsfluorescedunder blue excitation (BP450490/FT510/LP520), we followed the procedure of Weisse and Kenter (1991) and
used green excitation for enumerating all autotrophic picoplankton. This procedure may underestimate the abundance of eukaryotic picoplankton [see the
Results, and Weisse and Kenter (1991)].
Net population growth rates (g, per day) of microorganisms in each enclosure
were calculated as:
and
8t
= [in(c;g]/4
where Cn, C, and C, are the concentrations of a taxon or category initially, after 1
day and after 4 days, respectively; 1 and 4 are the incubation times in days.
686
Microbial food web of a mesotrophic lake
The effects of zooplankton biomass on growth rates were examined by simple
linear regression. Clearance rates, or the rates at which Daphnia and Boeckella
removed microorganisms from the water [ml \ig (dry wt)~' day~'], were derived
from the slopes of significant regressions (P < 0.05) that related microorganisms'
growth rate to zooplankton biomass (p^g dry wt I 1 ).
The effects of nutrients, zooplankton species and zooplankton density (excludes
enclosures without added zooplankton) were tested by three-factor ANOVA; the
effects of nutrients and zooplankton density on microbial abundance and clearance rates within zooplankton species, and including enclosures without added
zooplankton, were tested by two-factor ANOVA. All data were log transformed
before ANOVA to equalize variances.
Results
The concentrations of chlorophyll a, algae and microorganisms in Lake
Mahinerangi at the start of the experiment are shown in Table II.
Survival of the added zooplankton and their offspring in the enclosures at the
end of 4 days was very high (97-100%, except for one enclosure with 75%). In
addition to the added zooplankton, other small zooplankton at low densities were
retrieved from most of the enclosures after 4 days: B.hamata nauplii (0.2-3.5 1"')
and first instar copepodites (0.2^41"1), early copepodite instars of a small cyclopoid
(0-1.4 I"1) and small saccate rotifers, probably Synchaeta (0-8.2 I"1). Densities of
these 'other zooplankton' in the enclosures were not related to enclosure treatment (addition of nutrients, species and density of zooplankton).
Table II. Initial concentrations of chlorophyll a and microorganisms in Lake Mahinerangi at the start of
the experiment
Initial concentration (1 SE)
Algae
Chlorophyll a (jig I 1 )
(cells 1 ')
3.45
380 000
930
(0.116)
(70 000)
(128)
Picophytoplankton (cells ml 1 )
Red fluorescing (r-picoplankton)
Orange fluorescing (o-picoplankton)
11 090
4300
(530)
(230)
685 000
97 700
6900
782 700
(2470)
(890)
(860)
(2040)
Flagellates (cells ml 1 )
Heterotrophic nanoflagellates (HNF)
Photosynthetic flagellates (PF)
2950
12.75
(930)
(0.24)
Ciliates (cells 1"')
Large oligotrichs (>20 p.m)
Small oligotrichs (£20 jun)
Total ciliates
1258
400
2007
(190)
(118)
(322)
Cyclotella (cells I 1 )
Staurastrum, Staurodcsmus
Bacteria (cells m l ' )
Cocci (<1 p.m)
Small rods (<1 (j.m)
Large rods (~2 jim)
Total small bacteria (<1 p.m)
687
C.W.Bums and M.Schallenberg
301 N : <O.0O1 N : <0.001
Dns
B:n6
NxD ns
NxB: ns
OL
DL
BL
OH
DH
=•
20-
g
10
OL
BH
DL
300i
BL
OH
DH
BH
DH
BH
TREATMENT
TREATMENT
5001 N : p <0.001
N : p <0.001 N : p <0.001
D: ne
B :ne
NxD ns
NxB: ns
N : p <0 001
400
200
300
200
100
04
DL
BL
OH
TREATMENT
DH
BH
OL
DL
BL
OH
TREATMENT
Fig. 1. Nutrient concentrations (u.g I', ± 1 SE) in enclosures after 4 days. OL, DL and BL refer to low
nutrient (unenriched) enclosures without added zooplankton (OL), with added Daphnia (DL) and
with added Boeckella (BL); OH, DH and BH are high nutrient (enriched) enclosures without added
zooplankton (OH), with added Daphnia (DH) and with added Boeckella (BH). The results of twofactor ANOVA for treatment and interaction effects are shown in the top left of each graph, where N =
nutrients, D = Daphnia and B = Boeckella.
Nutrients
The effects of nutrient enrichment on the levels of soluble and total N and P are
shown in Figure 1. Nutrient enrichment significantly enhanced the concentrations
of inorganic and total N and P in the enclosures (three-factor ANOVA: all F values
for nutrient effects >24; all P = 0.0001), but there were no effects of zooplankton
species or density on these concentrations, nor was there any evidence of interactions between zooplankton and nutrients (all P > 0.2). As the nutrient concentrations in enclosures containing 2 adult Daphnia I"1 and 2 adult Boeckella I"1
did not differ significantly from those containing 8 H of the same species in the
same nutrient treatment, the zooplankton treatments were pooled within species
and nutrient treatments for two-factor ANOVA (Figure 1).
688
Microbial food web of a mesotrophic lake
Table DL Results of three-factor ANOVA on log-transformed concentrations in enclosures on day 4
for chlorophyll a (jig 1'). and days 1 and 4 for Cyclotella (cells ml"1). The analyses exclude treatments
without added zooplankton (OL and OH). Probabilities of 50.05 are shown in bold
d.f.
Nutrients (A)
Species (B)
AB
Density (C)
AC
BC
ABC
Error
1
1
1
1
1
1
1
16
Chlorophyll a D 4
Cyclotella Dl
Cyclotella D4
F
P
F
P
F
P
78.61
25.45
2.52
7.44
2.47
0.70
0.01
0.000
0.000
0.132
0.015
0.136
0.415
0.941
0.93
5.02
0.06
0.32
0.16
2.31
1.36
0.351
0.039
0.816
0.580
0.690
0.148
0.260
40.76
4.37
0.04
14.90
0.89
8.46
0J3
0.000
0.053
0.840
0.001
0.360
0.010
0.571
14-
N . p <0.001 N . p <0.001
D p <0.001 B : ns
NxD p=0.04 NxB: ns
12"
10'
8
6
OL
8DL
8BL
OH
8DH
8BH
TREATMENT
Fig. 2. Algal biomass, expressed as chlorophyll a (u,g I"1, ± 1 SE), in enclosures after 4 days. Abbreviations and the presentation of statistical results are as in Figure 1. Histograms for zooplankton treatments are for 8 animals I 1 .
Algae
Algal biomass, measured as chlorophyll a, increased after 4 days in response to
nutrients with zooplankton species and density also having significant effects
(Table III). After 1 day, a small species of Cyclotella (—10 jtm diameter), the most
abundant alga, was significantly lower in enclosures containing Daphnia than in
those with Boeckella (d.f. = 23, F= 5.23, P = 0.032). After 4 days, the concentrations of Cyclotella paralleled those of chlorophyll a, with significant effects of
nutrients, zooplankton species and density, and a significant interaction term
(Table III).
In enclosures without added zooplankton, chlorophyll a responded to nutrient
enrichment by increasing to 11 u,g I"1 which is >2.4 times that in the unenriched
enclosures (Figure 2). When the responses in chlorophyll a are related to zooplankton biomass, algal biomass declined with increasing Daphnia biomass in the
689
C.W.Bums and M.Sctiallenberg
presence and absence of added nutrients, but showed no significant responses to
Boeckella biomass (Figure 3A). The growth rate of Cyclotella followed the same
pattern, declining in the presence of Daphnia, but not Boeckella (Figure 3B). At
the highest Daphnia concentration (~330 jig I"1), this decline corresponded to the
daily removal of 37% of the Cyclotella cells.
Picophytoplankton
Two kinds of cells were distinguished based on their fluorescence with the green
filter set: those that fluoresced red, and were generally more abundant, and those
that fluoresced bright orange. Both are probably chroococcoid cyanobacteria that
differ in the composition, or proportions, of their main phycobiliproteins
(Reynolds, 1984; Maeda et ai, 1992; Weisse, 1993). We refer to the two types as
r-picoplankton (red-fluorescing) and o-picoplankton (orange-fluorescing).
The results of three-factor ANOVA for the effects of nutrients, zooplankton species and density on the abundance of eukaryotic picoplankton
(r-picoplankton) and prokaryotic picoplankton (o-picoplankton) after 4 days are
shown in Table IV. The abundance of r-picoplankton did not change in response to
nutrients, species of grazers or grazer density after 1 day (three-factor ANOVA,
all P > 0.5) or 4 days (Table IV); concentrations of r-picoplankton in enclosures
that lacked zooplankton did not differ significantly from those in enclosures with
added zooplankton (Figure 4).
Abundances of o-picoplankton in enclosures after 1 day showed weak, but significant, effects of zooplankton species (three-factor ANOVA, F = 4.56,
P = 0.048) and significant interaction terms (species x density; nutrients x species
x density: 0.01 < P < 0.05). After 4 days, concentrations of o-picoplankton were
lower in the presence of added nutrients, and lower in enclosures with Daphnia
than Boeckella, with significant interaction effects (Table IV). When enclosures
without added zooplankton are included in the analysis (two-factor ANOVA), the
effects of nutrients on o-picoplankton concentrations disappear, but there are significant effects of Daphnia and of Boeckella-nutrient interactions (Figure 4).
Bacteria
Heterotrophic bacteria consisted primarily of small cocci and rods <1.0 (xm, but
some large rods (~2 M-m), visible on primulin-stained filters with the UV filter set,
were present initially at densities of 7 x 103 ml 1 (Table II). After 1 day, there were
no significant changes in bacterial abundance related to nutrients, or to species or
density of zooplankton (three-factor ANOVA). Densities of small bacteria in the
enclosures increased significantly from 0.85 x 10* ml 1 (SE ± 0.03 x 106) on day 1
to 1.1 x 106 ml"1 (SE ± 0.06 x 10") on day 4 (P = 0.003). Concentrations of small
bacteria, large rods and total bacteria were significantly higher in nutrientenriched enclosures on day 4, although small bacteria and total bacteria were less
abundant in the presence of Daphnia than in the presence of Boeckella (Table V);
interactions between nutrients, species and density affected the concentrations of
small bacteria and total bacteria.
When the enclosures without zooplankton were included in the analysis, there
were no measurable effects of nutrients, Daphnia or Boeckella on the abundance
690
Microbial food web of a mesotrophic lake
100
200
300
400
ZOOPL BIOMASS (jig^)
1.01
B
o
u
100
200
300
400
ZOOPL BIOMASS (ugfl)
Fig. 3. Relationship between algal indices and zooplankton biomass of Daphnia (circles) and Boeckella
(squares) in nutrient-enriched (solid symbols) and unenriched (open symbols) enclosures. Linear
regression lines were fitted to the data for each species and are shown for Daphnia, which is the only
species for which the relationships were statistically significant (P<,0.05). (A) Regressions relating
chlorophyll a (y, in p.g I -') to biomass of added Daphnia (x, in ng I 1 ) in enriched enclosures, when
y = 10.194 - 0.0173J: (r2 = 0.642), and in unenriched enclosures, wheny = 3.8566 - 0.00397* (r2 = 0.524).
(B) Regressions relating net growth rate (y, as g d a y ' ) of Cyclotella to biomass of added Daphnia (x, in
jig I 1 ) in nutrient-enriched enclosures, when y = 0.77028 - 0.00113x (r2 = 0.758) and in unenriched
enclosures, when y = 0.44398 - 0.00096* (r2 = 0.763).
of small bacteria after 4 days (Figure 5), although net growth rates of cocci and
small rods increased with increasing Boeckella biomass in the enriched enclosures
(cocci: r2 = 0.408, P = 0.064; rods: r> = 0.636, P = 0.01).
The large rods multiplied during the 4 day incubation period to attain densities,
in the absence of Daphnia, of —10 x 103 ml 1 in the unenriched enclosures and
30 x 103 ml"1 in the enriched enclosures. In the unfertilized treatments, they comprised 0.8% of the total bacterial abundance on days 1 and 4; in the enriched
enclosures, this percentage increased from 0.9% on day 1 to 2.4% on day 4.
Boeckella had no effect on the abundance of these rods (Figure 6). Net growth
691
CW.Burns and M^challenberg
Tabk IV. Results of three-factor ANOVA on log-transformed abundances (numbers ml 1 ) of orangefiuorescing photosynthetic picoplankton (o-pico), red-fluorescing picoplankton (r-pico), heterotrophic
nanoflagellates (HNF) and photosynthetic flagellates (PF) in enclosures on day 4. The analyses exclude
treatments without added zooplankton (OL and OH). Probabilities of £0.05 are shown in bold
d.f.
Nutrients (A)
1
1
Species (B)
AB
1
Density (C)
1
AC
1
1
BC
ABC
1
Error
16
o-pico
PF
HNF
r-pico
F
P
F
P
F
P
F
P
7.15
13.6
1.69
1.91
1.50
0.01
10.2
0.017
0.002
0.213
0.186
0.238
0.922
0.006
1.46
0.27
0.10
0.17
0.%
3.64
0.89
0.245
0.614
0.761
0.681
0.343
0.075
0.358
1.53
0.14
0.27
1.77
1.06
0.00
0.501
0.235
0.709
0.611
0.202
0.318
0.972
0.489
9.78
0.13
0.69
1.90
0.064
2.84
0.178
0.006
0.725
0.419
0.187
0.804
0.111
0.679
rates of these rods declined with increasing Daphnia biomass in the presence and
absence of added nutrients (Figure 6).
Flagellates
The abundance of heterotrophic nanoflagellates (HNF) in the enclosures ranged
from 1300 to 5400 ml'; most were <5ujn. Variances within treatments were high
and there were no measurable changes in HNF abundance in response to nutrients
or zooplankton after 1 or 4 days and no significant nutrient-zooplankton interactions (Table IV, Figure 7). A large photosyntheticflagellate(PF) declined in abundance throughout the experiment, but was more abundant in nutrient-enriched
enclosures after 4 days than in enclosures without added nutrients (Table IV,
Figure 7). In nutrient-enriched enclosures, the growth rates of HNF after 4 days
declined with Daphnia density and those of the photosynthetic flagellate declined
with increasing Boeckella biomass (Figure 7).
Ciliates
Oligotrichs (Strombidium, Strobilidium, Halteria) comprised 83% of the total
ciliates in Lake Mahinerangi (Table II). Approximately 76% of these oligotrichs
were >20 u.m in length; the largest ciliate was Paradileptus. The effects of zooplankton and nutrients on ciliate abundances after 1 and 4 days are shown in Figure
8. When enclosures lacking added zooplankton are omitted from the analysis
(three-factor ANOVA), there were no significant changes in total ciliate abundance in response to nutrient enrichment after 1 day (F = 0.054, P = 0.818) and 4
days (F = 3.44, P = 0.080). There were, however, significant effects of zooplankton
species, density and species-density interactions on ciliate abundance after 1 day
(three-factor ANOVA, all P < 0.02) and 4 days (all P ^ 0.0005).
The growth rates of total ciliates after 1 day were unrelated to the presence of
Daphnia, but decreased after 4 days with increasing Daphnia biomass in the presence and absence of added nutrients (Figure 9). Boeckella had highly significant
692
MicTobial food web of a mesotrophic lake
OL
DL
BL
OH
DH
TREATMENT
Nns
100001 N r s
D : p <0.01 B: ns
NxD ns
NxB p <0 05
8000"
O
6000"
3
4000
2000
OL
DL
BL
OH
DH
BH
TREATMENT
Fig. 4. Autotrophic picoplankton (ml"', ± 1 SE) in enclosures after 4 days, r-picoplankton = red-fluorescing cells; o-picoplankton = orange-fluorescing prokaryotic cells under a greenfilterset (see the text).
Abbreviations and the presentation of statistical results are as in Figure 1.
negative effects on total ciliate population growth after 1 and 4 days, in nutrientenriched and unenriched enclosures (all P < 0.001).
To ascertain whether Boeckella depressed the population growth rates of large
oligotnchs more strongly than those of small oligotnchs, which might be the case if
Boeckella fed selectively on larger ciliates, the relationships between Boeckella
biomass and oligotrich growth rates after 4 days were examined separately for
oligotrichs that were £20 p.m (small) and >20 u.m (large) in the two nutrient treatments. The net growth rates of small ciliates were less than those of large ciliates
(Figure 10). In the unenriched enclosures, the slope of the regression line for
growth rate of large ciliates was significantly steeper than that of small ciliates
(one-tailed r-test for differences between the slopes of the regression lines: t = 2,
P < 0.05), but in the enriched enclosures the slopes of the regression lines did not
differ (/= 1.472, P> 0.05).
693
C.W.Buras and M-Schallenberg
Table V. Results of three-factor ANOVA on log-transformed concentrations (numbers ml ') of small
bacteria (< I u.m). large rods and total bacteria in enclosures on day 4. The analyses exclude treatments
without added zooplankton (OL and OH). Probabilities of £0.05 are shown in bold
df
Nutrients (A)
Species (B)
AB
Density (C)
AC
BC
ABC
Error
Small bacteria
Large rods
Total bacteria
F
P
F
P
F
P
5.133
4.37
2.80
1.08
1.72
0.02
8.23
0.038
0.053
0.113
0.314
0 209
0.877
0.011
51.99
2.75
0.00
3.66
0.87
1.89
1.09
0.000
0117
0.994
0.074
0.365
0.188
0.313
6.16
4.60
2.84
0.91
1.54
0.04
8.52
0.025
0.048
0.111
0.354
0.232
0.854
0.010
1(
2.01
DAY 4
N . ns
Dns
NxD: ns
DAY1
OL
8DL
8BL
OH
N: ns
B:ns
NxB: ns
8DH
8BH
TREATMENT
Fig. 5. Bacteria (x l0*ml ', ± I SE) in enclosures after 1 day (open columns) and 4 days (solid columns).
Abbreviations and the presentation of statistical results are as in Figure I. Histograms for zooplankton
treatments are for 8 animals I '.
The weight-specific rates at which Daphnia and Boeckella cleared microorganisms from the water are shown in Table VI. Clearance rates for small particles
<10 [Lm (bacteria, flagellates, Cyclotella) are lower than those for ciliates. Boeckella cleared ciliates from the water at rates of 3.18-5.85 ml \ig (dry wt)-' day 1 ,
which are an order of magnitude higher than those at which Daphnia removed
ciliates.
Keratella was the only small rotifer present in the enclosures (Figure 11). Abundances ranged from 0 to 56 rotifers I 1 , but were unrelated to enrichment, species or
concentration of crustacean zooplankton (three-way ANOVA, all P > 0.3).
Discussion
In studies of complex food web interactions in lakes, it is tempting to impose perturbations that are unrealistically large in order to ensure measurable outcomes.
694
Microbial food web of a mesotrophic lake
401
N:p<0.001
D:p<0.01
NxD ns
N:p<0001
Bns
NxB: ns
»
A
30'
I
20-
O
10-
OL
8DL
8BL
OH
8DH 8BH
TREATMENT
B
100
200
300
400
ZOOPL BIOMASS (ug/1)
Fig. 6. (A) Large rod-like bacteria (x 10-' ml"1, ± 1 SE) in enclosures after 4 days. Abbreviations and the
presentation of statistical results are as in Figure 1. Histograms for zooplankton treatments are for 8
animals I 1 . (B) Relationship between net daily growth rates of large rods (y, as g day-') in enclosures on
day 4, and Daphnia biomass (x, in (ig I'). In enriched enclosures (black circles), y = 0.4643 - 0.00076*
(H = 0.387, P = 0.0734); in unenriched enclosures (open circles), y = 0.06773 - 0.00063* (r2 = 0.450,
P = 0.0478).
Whereas the results of extreme 'presses' may shed light on processes and pathways
involved in ecosystem functioning, they cannot readily be extrapolated to describe
the relative importance of the various interactions in the lake itself. In our study,
the concentrations of TN, TP and zooplankton in the enclosures at the end of the
incubation period fall within the range of concentrations that have been recorded
in Lake Mahinerangi (Malthus, 1986; Burns, 1992). For this reason, the scope and
scale of the responses of the microbial community in the enclosures are likely to be
realistic reflections of those that occur in the lake.
Responses after 1 day—top-down effects
Our objective in sampling the enclosures after 1 day was to identify and separate
the dominant top-down effects of Daphnia and Boeckella on algae and the
microbial community from the combined effects of consumption (top-down) and
695
C.W.Bums and M-Schallenbcrg
N : p <0.01 N : p <0 06
Dns
Bns
MxDire
NxBrs
8OOO
7000 •
B
6000
500040003000
2000
1000
OL
OH
a
OH
BH
DH
DL
TREATVBfT
BH
TREATNBCT
c
0.3
4
BM-
I",
z 0.0
I
m
-01
\
m
100
200
300
ZOOPL BIOUASS (|igfl)
400
100
200
300
400
ZOOPL BIOMASS Ctg/I)
Fig. 7. (A) and (B) Flagellates (ml 1 , ± 1 SE) in enclosures after 4 days. HNF= heterotrophic nanoflagellates (A); PF = photosynthetic flagellate (B). Abbreviations and the presentation of statistical
results are as in Figure 1. (C) and (D) Relationship between net growth rates of flagellates (g day-') in
enriched enclosures on day 4, and zooplankton biomass (jig 1 ') of Daphnia (circles) and Boeckella
(squares). (C) Regression line relating net growth rate of heterotrophic nanoflagellates (y) to Daphnia
biomass (*), where y = 0.1586 - 0.000665* (^ = 0.430, P = 0.055). (D) Regression line relating net
growth rate of a photosynthetic flagellate (y) to Boeckella biomass (x), where y = 0.154 - 0.002607*
(r2 = 0.854, P< 0.001).
nutrient enhancement (bottom-up) after 4 days. Through their feeding activities,
Daphnia and Boeckella exerted two different, and strong, top-down effects on the
microorganisms in Lake Mahinerangi. Adult D.carinata at moderate densities
(2-81"1) lowered the concentration of the dominant alga, Cyclotella, significantly,
but had no measurable impact on any components of the microbial food web. In
contrast, Boeckella reduced the concentration of ciliates severely and had no
measurable direct effects on other microorganisms, or algae. These responses are
consistent with the well-documented prowess of large Daphnia to clear algae from
water in short-term grazing experiments (reviewed by Lampert, 1987) and
recently documented abilities of freshwater calanoids (Diaptomus spp.,
Epischura) to cull ciliates (Burns and Gilbert, 1993; Hartmann etal., 1993; Wiackowski et al., 1994).
6%
Microbial food web of a mesotrophic lake
50001 DAY1
N rts
B: p < 0 001
NxB:ns
4000-
DAY 4
N : p < 0.05
D : p < 0 006
NxDns
N:ns
B:p<0.001
NxBns
3000
2000
1000
OL
8DL
8BL
8DH
8BH
TREATMENT
Fig. 8. Total ciliates (number 1', ± 1 SE) in enclosures after 1 day (open columns) and 4 days (solid
columns). Abbreviations and the presentation of statistical results are as in Figure 1. Histograms for
zooplankton treatments are for 8 animals I 1 .
Responses after 4 days—bottom-up effects
The strong positive effects of inorganic nutrient additions on the levels of soluble
inorganic N and P and total N and TP in the enriched enclosures (Figure 1) confirm
that the enrichment procedures were successful. The presence of crustaceans in
the enclosures had no effects on concentrations of NH4-N and PO4-P after 4 days,
probably because the highest biomass of zooplankton used (—330 (ig 1"') was too
small for rates of nutrient remineralization to be detected, and because inorganic
nutrients released by excretion and egestion of the zooplankton are taken up
rapidly by algae. In a study of nutrient recycling by crustacean zooplankton in
Lake Washington, Lehman (1980) found that enclosures enriched with >600 ng
(dry wt) I"1 of Daphnia and copepods had higher concentrations of NH4-N, PO4-P
and dissolved P after 2 days than those containing 40-160 (xg 1~' zooplankton, but
that these differences disappeared after 3 days. In mesotrophic Castle Lake, Elser
and Goldman (1991) detected no increase in SRP after 4 days in enclosures containing 425 n-g \~l Daphnia, although NH4-N increased. As the highest biomass of
added zooplankton in our study was —330 u.g I"1, and the period of in situ enclosure
was 4 days, we did not expect to find differences in nutrient concentration that
could be related to differences in zooplankton biomass, although increases in soluble inorganic N, associated with the presence of Daphnia, and increases in SRP,
associated with the presence of Diaptomus, have been reported in enclosures after
8 days (Brett et ai, 1994).
The addition of nutrients had positive effects on algal biomass and the growth
rates of a small diatom, Cyclotella, a large photosynthetic flagellate, and bacteria,
but no measurable effects on the abundance of r-picoplankton, HNF and ciliates
(Table VII). The strong stimulatory effect of nutrient additions on the growth of
Cyclotella indicates that it was nutrient limited and is consistent with the low concentrations of soluble inorganic nutrients in Lake Mahinerangi at the time of the
study. In contrast, r-picoplankton did not respond to nutrient enrichment, which
697
C.W.Bums and M^challenberg
02-
OAY1
LOWNUTTBQfTS
0.0-
°
A
-021
•oV
-06
-08
•10
•12
100
200
300
400
100
ZOOPL BtOWASS (p»fl)
200
300
ZOOPL BIOMASS (Mflfl)
DAY1 HCHNUmBENTS
c
L KB
3
»
CO
-04
3 -08
0
• \
0
\
•
°\
, • N—,
200
100
300
ZOOPL BtOIIASS (MB/0
100
200
300
ZOOPL BtOUASS (Jltfi)
Fig. 9. Relationship between net growth rates (y, as g day 1 ) of ciliates on days 1 and 4 and zooplankton
biomass (x, in jig 1') in unennched (low nutrients) and enriched (high nutrients) enclosures. Linear
regressions were fitted to the data for Daphnia (open circles) and Boeckella (solid squares); regression
lines are shown only when the relationships are statistically significant (Pi 0.05). After 1 day, ciliate
growth rate decreased with increasing Boeckella biomass in unenriched enclosures (A) asy = -0.242 0.0058&r (H = 0.884), and in enriched enclosures (C) as y = -0.1793 - 0.005341* (r2 = 0.841). After 4
days, ciliate growth rate decreased in unenriched enclosures (B) with increasing Boeckella biomass as
y = 0.07297 - 0.00451 \x (r2 = 0.871), and with increasing Daphnia biomass as y = 0.3353 - 0.00051*
(r* = 0.575); in enriched enclosures (D), ciliate growth rate decreased with increasing Boeckella biomass as y = 0.1352 - 0.0041 ]6x (r2 = 0.911), and with increasing Daphnia biomass as y- 0.1132 0.00043001(^ =
suggests that they were not nutrient limited, or that any nutrient-stimulated population growth was balanced by losses of cells to grazers. The negative response of
o-picoplankton to nutrients in the presence of zooplankton implies that enrichment affected them adversely in addition to a depression in their population
growth caused by Daphnia. The hypothesis that high nutrient levels may depress,
rather than stimulate, population growth of picoplankton is consistent with observations that picoalgal abundance tends to decrease with increasing lake trophy
(Stockner and Antia, 1986; Burns and Stockner, 1991), and competitive
superiority of eukaryotes over prokaryotes in the ability to take up nutrients from
enriched waters (Weisse, 1993), although changes in abundance and species of
grazers accompanying eutrophication cannot be ruled out. Some evidence suggests that the relatively low N:P ratio in the fertilized enclosures (12:1) may selectively favour eukaryotic algae rather than prokaryotic picoplankton. Chemostat
698
Microbial food web of a mesotropbic lake
0.4
LOW NUTRIENTS
A
0.2J
I
X
5
OOtl
-02-0.4 •
-0.6
D
-0.8
100
200
BOECKELLA BIOMASS (jig/1)
HIGH NUTRIENTS
B
200
BOECKELLA BIOMASS (ng/1)
Fig. 10. Relationship between net growth rates (g day 1 ) of oligotrich ciliates on day 4 and Boeckella
biomass (u.g I ') in unenriched (low nutrients) and enriched (high nutrients) enclosures. Linear
regressions were fitted to the data for small oligotrichs (£20 u.m, open squares) and large oligotrichs
(>20 u.m, solid squares). (A) Low nutrients. Net growth rates (y) of small oligotrichs decreased with
Boeckella biomass (x) as y = -0.12201 - 0.00362.V (r' = 0.672. P = 0.007); net growth rates of large oligotrichs decreased as y = 0.13701 - 0.00541* (r2 = 0.842, P< 0.001). (B) High nutrients. Net growth
rates (y) of small oligotrichs decreased with Boeckella biomass (jr) as y = -0.2694- 0.003 \&x(r> = 0.397,
P = 0.069); net growth rates of large oligotrichs decreased as y = 0.22598 - 0.0O478J (r* = 0.922,
P< 0.001).
studies with natural plankton showed that Synechococcus dominated at a N:P supply ratio of 20, whereas diatoms and Scenedesmus dominated at ratios of 2 and 7
(Pick and Lean, 1987).
Bacteria have high affinity for inorganic N and P [e.g. Caron et al. (1988) and
references therein]. It is not surprising, therefore, that nutrient additions stimulated bacterial population growth rates after 4 days. Bacterial growth was
enhanced by nutrients only in the presence of zooplankton (Table V) and not when
zooplankton were absent (Figure 5), probably because protistan grazers, primarily
699
C.W.Bums and M.SchaUenberg
Table VI. Clearance rates [ml jig (dry wt)~' day 1 ] derived from the slopes of significant regressions
(P <, 0.05) that relate growth rate negatively to biomass of Daphnia and Boeckella. L and H refer to
enclosures without (L) and with (H) added nutrients
Daphnia
Algae
Chlorophyll a
Cyclotella
Picophytoplankton
r-picoplankton
o-picoplankton
Bacteria
Large rods
Flagellates
HNF
PF
Ciliates
Total, day 1
Total, day 4
Boeckella
L
H
L
H
0.29
0.96
0.6
1.13
-
-
-
0.68
0.63
0.76
_
-
0.66
-
_
2.6
0.51
0.43
Oligotrichs 220 JJUTI
Oligotrichs >20 u.m
0.42
5.85
4.51
3.61
5.4
5.34
4.12
3.18
4.77
heterotrophic flagellates and ciliates, were more abundant in enclosures that
lacked zooplankton and were suppressing the bacteria (see below).
Responses after 4 days—top-down effects
When present at a density of 8 adults I"1 for 4 days, Daphnia strongly depressed
algal biomass and the growth rate of Cyclotella. Daphnia cleared Cyclotella from
the water at rates of 0.96-1.13 ml u-g (dry wt)-' day 1 (Table VI) or ~2 ml Daphnia-*
rr1. The adult D.carinata in Lake Mahinerangi were relatively large (1.87 mm) and
this rate is similar to maximum rates recorded for other large-bodied Daphnia
(Lampert, 1987). In contrast, Boeckella at the same density had no impact on algal
biomass or the growth rate of Cyclotella after 4 days. Several factors may have
contributed to this difference between Daphnia and Boeckella in their impact on
phytoplankton. (i) Calanoid copepods feed selectively and prefer large to small
algae so that their weight-specific clearance rates for small algae are lower than
those of less selective daphniids. When exposed to monocultures of algae at low
concentration, female B.hamata clear Cyclotella and Cryptomonas at maximum
rates of 0.2-0.7 ml animal"1 h"1 (Burns and Xu, 1990a; Burns and Hegarty, 1994)
compared to 3-10 times this rate for large D.carinata (this study; Ganf and Shiel,
1985). Even at these maximum rates, and not allowing for algal growth, Boeckella
at a density of 8 females I"1 would clear Cyclotella from <14% of an enclosure in a
day. (ii) Adult Boeckella are smaller and weigh less than adult D.carinata so that 8
Boeckella I"1 had approximately the same biomass as 2 Daphnia I-1; this latter daphniid density had no measurable impact on algal biomass or Cyclotella growth rate.
700
Microbial food web of a mesolrophic lake
^
BL
OH
BM
TREATMENT
1
Fig. 11. Keratella (number I- , ± 1 SE) in enclosures after 1 day (open columns) and 4 days (shaded
columns). Abbreviations are as in Figure 1.
Therefore, we cannot discount the possibility that higher densities of Boeckella
(~330 u.g I"1 or 22 adult females 1"') may also have had detectable top-down effects
on Cyclotella.
The absence of any detectable response of r-picoplankton to the presence of
crustaceans is consistent with low rates of clearance of autotrophic picoplankton
by Daphnia and Diaptomus (Bogdan and Gilbert, 1984; Lampert and Taylor, 1985;
Fahnenstiel et ai, 1991). However, grazing by Daphnia probably accounts for the
negative effect of this cladoceran on the growth rate of o-picoplankton in the
enriched enclosures. Although the dominant consumers of coccoid cyanobacteria
are likely to be smallflagellatesand ciliates (e.g. Fahnenstiel etal., 1991), Daphnia
removed Synechococcus in Schdhsee (Lampert and Taylor, 1985) and o-picoplankton have been observed in enormous numbers in the guts of cladocerans
(Burns and Stockner, 1991). As Daphnia have poor ability to feed selectively
(Lampert, 1987), and hence are unlikely to be able to discriminate between r- and
o-picoplankton, we attribute their significant negative effect on o-picoplankton
and non-significant effect on r-picoplankton to high variances of the r-picoplankton data that increase the probability of a Type II error. Other explanations are
possible, however. Picoplankton are at the lower end of the size range of particles
that most large Daphnia can remove efficiently (B0rsheim and Andersen, 1987;
Lampert, 1987). The o-picoplankton cells may have been slightly larger than those
of the r-picoplankton and hence have been retained more efficiently by D.carinata.
The average net growth rates of ciliates in enclosures over the first 24 h were
negative, even in the absence of added crustaceans (Figure 9). These net negative
rates may reflect the sensitivity of some ciliates to containment (Taylor and
Johannsson, 1991). For example, Strombidium disappeared at rates of -0.77 to
-0.2 day-' from enclosures in Lake Michigan (Carrick et al., 1992); it was also
present in our enclosures. The multiplication of more robust species during the
4 day incubation in Lake Mahinerangi resulted in positive mean growth rates for
ciliates >20 u.m in enclosures without added zooplankton of 0.03 day 1 (no added
nutrients) to 0.14 day 1 (enriched). Although low relative to the potential rates of
increase of oligotrichs in the presence of abundant food (Taylor and Johannsson,
1991), these rates fall within the range of 0-1.4 day 1 which have been recorded for
701
C.W.Bums and M.Scfiallenberg
Table VII. Summary of responses of microbial food web organisms in Lake Mahinerangi to nutrients
and crustacean grazers after 4 days Signs indicate statistically significant (P<0.05) increases (+).
decreases (-) or no changes (NS) in abundance or net growth rate in nutrient-enriched enclosures
relative to unenriched enclosures and in nutrient-enriched enclosures with grazers relative to nutrientenriched ones without grazers (ANOVA, or linear regression*)
Response to
Nutrients
Grazers
Daphnia
Boeckella
Algae
Chlorophyll a
Cyclotella
+
+
-
NS
NS
Picophytoplankton
Red-fiuorescing
Orange-fluorescing
NS
NS
NS
NS
NS
Bacteria
Cocci
Small rods
Large rods
Total small bacteria
NS
NS
+
NS
NS
NS
+*
+*
NS
+*
Flagellates
HNF
PF
NS
+
_*
NS
NS
Ciliates
Large oligotnchs
Small oligotrichs
Total ciliates
NS
NS
NS
NS
_*
NS
ciliates in Lakes Michigan and Ontario (Taylor and Johannsson, 1991; Carrick et
al., 1992). Factors that may have contributed to the relatively low net growth rates
in our experiments are: (i) differential sensitivity of species to containment; (ii) differential growth rates of ciliates (Carrick etal., 1992) and the possible domination
by slow-growing species; (iii) the temperature at the time of the study (13°C); (iv)
resource limitation (see below); (v) predation. Potential metazoan predators of
ciliates (small saccate rotifers, nauplii and early copepodites) were relatively
sparse in our enclosures (<91 '), but in view of their ability to clear ciliates at rates
of up to -20 ml animal-1 day-' (Burns and Gilbert, 1993; Gilbert and Jack, 1993),
they cannot be dismissed as potential contributors to the low net rates of ciliate
growth.
After 4 days in the presence of Daphnia, densities and growth rate of ciliates
were depressed (Table VII). Negative effects of Daphnia on ciliates have been
reported in several studies (Porter et al., 1979; Carrick etal., 1991; Pace and Funk,
1991; Wickham and Gilbert, 1991,1993; Jack and Gilbert, 1993,1994; Brett etal.,
1994; Wiackowski etal., 1994). In our study, D.carinata did not suppress small and
large ciliates differentially according to size, as has been noted in other studies
(Wickham and Gilbert, 1993; Jack and Gilbert, 1994; Wiackowski et al., 1994). In
studies in Star Lake, populations of small ciliates were depressed by D.pulex more
than those of large ciliates (Wickham and Gilbert, 1993; Jack and Gilbert, 1994),
whereas large ciliates were affected more than small ones by the Daphnia in Castle
702
Microbial food web of a mesotrophk lake
Lake (Wiackowski et al., 1994). Several factors may account for a lack of differential response between small and large ciliates in the presence of Daphnia in our
study, and for the difference in effects of Daphnia in the studies cited above: (i)
different authors use different size thresholds between 'large' and 'small' ciliate
categories (e.g. —30 ^m for Wiackowski etal., 1994; 20 \im in our study); (ii) different intrinsic rates of increase between large and small ciliates; (iii) species-specific
differences among ciliates in the ability to avoid competition (exploitative or interference), or consumption, by Daphnia that are unrelated to size (Jack and Gilbert,
1993; Wickham and Gilbert, 1993).
Daphnia can lower the growth rates and abundance of ciliates directly by predation, interference, or both, and indirectly by exploitative competition for the
same food resource [Jack and Gilbert (1994) and references therein]. The rates at
which D.carinata removed ciliates from the water in enriched and unenriched
enclosures [0.43-0.51 ml (xg (dry wt)~' day 1 ] are slightly less than those at which
they cleared Cydotella (Table IV), which is consistent with ciliates being an
'incidental catch' in the inhalant current of Daphnia during their routine collection
of algae and with avoidance behaviours of some ciliates (Jack and Gilbert, 1993;
Wickham and Gilbert, 1993). This interpretation accounts for a daphniid effect on
ciliates being detected after 4 days at the highest daphniid density, but not after 1
day. The clearance rates for ciliates that we measured would have allowed daphniid densities of 8 I"1 to remove ciliates from only 15% of the volume of an enclosure after 1 day, and 2 Daphnia V to remove ciliates from the same volume after 4
days.
In contrast, Boeckella at 2 and 8 animals I 1 had strong negative effects on ciliate
abundance and growth after 1 and 4 days. This difference is reflected in weightspecific clearance rates that are an order of magnitude higher than those of
Daphnia (Table VI) and per capita rates that are 3-4 times higher than those of
Daphnia. Boeckella is a suspension feeder that grows and reproduces well on
purely algal diets (Burns and Xu, 1990b; Xu and Burns, 1991). Our finding that
Boeckella has a much stronger negative effect on ciliates than Daphnia differs
from that of Brett et al. (1994) and Wiackowski et al. (1994), who found that Daphnia rosea was as effective as the calanoid, Diaptomus novamexicanus, in Castle
Lake in depressing ciliate growth. Daphnia were also more effective than copepods in depressing ciliates in enclosures in mesotrophic Schohsee (JUrgens et al.,
1994a), although the effects of a calanoid (Eudiaptomus gracilis) cannot be separated from those of equally numerous cyclopoids (Thermocyclops oithonoides,
Cyclops kolensis, Cyclops abyssorum). Our finding that Boeckella removed large
ciliates (>20 jun) faster than small ones in enriched enclosures (Figure 10) is consistent with those of others who have reported that large ciliates are affected by
crustacean zooplankton more adversely than small ones (Arndt and Nixdorf, 1991;
Wiackowski et al., 1994).
Flagellates are generally considered to be the major food resource of oligotrich
ciliates, although bacteria and autotrophic picoplankton are also consumed, sometimes at high rates (reviewed by Laybourn-Parry, 1992). If the ciliate populations
in Lake Mahinerangi were regulating flagellate abundance through predation
(top-down control), we might expect tofindan inverse relationship between flagel703
C.W.Burns and M-Schallenberg
late abundance and ciliate abundance. There was no correlation (P > 0.5). Instead,
ciliate numbers increased with flagellate abundance in the nutrient-enriched
enclosures (log-transformed data, n = 15, r2 = 0.2914, P = 0.0378), which implies
that ciliate abundance may have been determined, in part, by HNF availability.
There was no significant relationship between ciliate and flagellate populations in
the unenriched enclosures, presumably because HNF were resource limited themselves (see below).
The mean net growth rate of HNF in Lake Mahinerangi in the absence of crustaceans, 0.15 day 1 (Figure 7), falls within a range of 0.04-0.29 day 1 for HNF in
Lake Michigan during the spring isothermal period (Carrick etal., 1992) and is at
the lower end of a range of rates reported for HNF in mesotrophic Lake Constance
in early summer (Weisse, 1991). Growth of HNF did not change in the presence of
Boeckella, probably because copepods feed inefficiently on particles in the size
range of the small (2-5 n,m) HNF which predominated (Sherr et al., 1986; Bogdan
and Gilbert, 1987). In the presence of Daphnia, the growth rate of HNF decreased
in the enriched enclosures (Table VII). As HNF growth rates were not depressed
by Daphnia in the unenriched enclosures, which contained fewer bacteria for them
to feed on, it is unlikely that suppressed rates in the presence of Daphnia were an
indirect consequence of exploitative competition between Daphnia and flagellates
for bacterial food resources; rather, the low HNF growth rates are likely to be a
direct consequence of larger volumes of water cleared by Daphnia in the enriched
enclosures (Table VI) and hence greater rates of consumption of HNF by Daphnia
(top-down control). Christoffersen et al. (1993) report cladoceran control of HNF
in eutrophic conditions.
As an indirect indication of whether bacterial abundance might be limiting
flagellate population growth in Lake Mahinerangi, correlations were carried out
between HNF density and bacterial abundance in the presence and absence of
added nutrients. HNF density was positively correlated with bacterial abundance
in enclosures without added nutrients (n = 15, r = 0.580, P = 0.0235), but not in
those with added nutrients. These results imply a strong coupling between bacteria
and HNF that is broken by increased nutrient enrichment. A positive correlation
exists between nanoplankton and bacteria over a wide variety of freshwater
habitats and latitudes, and is consistent with a predator-prey interaction between
HNF and bacteria (Berninger et al., 1991). Heterotrophic flagellates have been
identified as the major consumer of bacteria in lakes, particularly when Daphnia
are scarce (e.g. Sanders et al., 1989; Pace et al., 1990; Fukami et al., 1991). Strong
coupling between HNF and bacteria at certain times of the year has also been
inferred from studies in a variety of lakes (e.g. Nagata, 1988; Bloem and
BSr-Gilissen, 1989; Weisse, 1991), although not in others (e.g. Pace and Funke,
1991; Carrick et al., 1992). Based on mean densities of bacteria and HNF in the
unenriched enclosures of 1.13 x 106 bacteria ml 1 and 3000 HNF ml 1 , respectively
(Figure 5), and a mean grazing rate of 15 bacteria HNF-1 Ir1 (Jurgens and Stolpe,
1995), the HNF in Lake Mahinerangi could remove 95% of the bacterial standing
stock per day. Even if the flagellate grazing rates were considerably lower (2 nl
flagellate-1 h~'; Jurgens, 1994), HNF still had approximately twice the potential of
Daphnia to control bacterial abundance in Lake Mahinerangi (top-down control).
704
Microbial food web of a mesotrophic lake
Daphnia at 8 I"1 (the highest biomass in our study) would only have removed
~8-27% of the standing stock of bacteria, based on rates of bacterial clearance by
1.87 mm Daphnia of 0.4 ml animal1 h"1 (Jtirgens and Stolpe, 1995) or 1.4 ml animal 1 h 1 (Porter et al., 1983).
Our finding that the correlation between HNF and bacterial abundance disappeared in the enriched enclosures is consistent with the hypothesis that the HNF in
Lake Mahinerangi are resource (bacteria) limited (bottom-up control). Berninger
et al. (1991) concluded that the abundance of heterotrophic nanoplankton in
nutrient-poor systems is largely determined and controlled by the abundance of
bacteria; Andersen and S0rensen (1986) drew similar conclusions from their study
of a eutrophic, coastal marine environment. In Lake Constance, the production of
HNF appears to be limited in spring by the availability of bacteria (Weisse, 1991).
The growth of HNF in our study appears to have been controlled from below when
levels of inorganic nutrients were low, and from above at high nutrient levels.
The biomass-specific clearance rates of Daphnia and Boeckella for flagellates
and ciliates in Lake Mahinerangi ranged from 0.42 to 5.85 ml u-g (dry wt)-' day-'
(Table VI). This range is similar to that of 0.4-5.2 ml jxg (dry wt)"1 day-' recorded
for the clearance of flagellates and ciliates by macrozooplankton, primarily
Diaptomus and Daphnia, in Lake Michigan (Carrick et al., 1991). The biomassspecific clearance rate of D.carinata for the smallflagellatesin Lake Mahinerangi,
0.66 ml (ig (dry wt)-' day 1 , which we calculated from the slope of the regression
relating daphniid biomass to net growth rate of HNF (Table VI), lies within a range
of biomass-specific rates of 0.46-0.77 ml fxg (dry wt) 1 day 1 for adult D.magna and
D.hyalina feeding on the colourless chrysomonad Spumella (JUrgens and Stolpe,
1995). The biomass-specific clearance rates (Table VI) can be used to calculate the
proportions offlagellateand ciliate standing stocks consumed by macrozooplankton per day. When present at densities of 8 individuals I"1 D.carinata consumed
19.8% of the HNF standing stock and 13-15% of the standing stock of ciliates per
day. This estimate for ciliate consumption falls near the lower end of the range for
Daphnia grazing on Strobilidium sp. in Storrs Pond, NH (Wickham and Gilbert,
1993) and is considerably higher than the 2.8% of ciliate standing stock consumed
by macrozooplankton in Lake Constance (Weisse, 1990).
In contrast to Daphnia, Boeckella at a density of 81"1 consumed between 49 and
70% of ciliate standing stock per day. If the ciliates in Lake Mahinerangi are primarily algivorous, as the dominance of oligotrichs implies (Fenchel, 1980), our
finding that they are consumed so effectively by Boeckella suggests the existence of
a strong nanoplankton-ciliate-calanoid coupling in this lake. Comparable couplings may also occur in lakes containing diaptomids. Equations that relate the rates
at which copepods clear ciliates to calanoid body size (prosomal length) have been
derived for species of Diaptomus and Epischura (Burns and Gilbert, 1993). The
rates at which adult female B.hamata cleared ciliates from Lake Mahinerangi
(Table VI) are equivalent to per capita rates of 48-88 ml animal"1 day*1 and bracket
the rate of 68 ml animal"1 day-1 that is predicted for a diaptomid of the same mean
prosomal length of the B.hamata in our study (1.06 mm). Thus, Boeckella and
Diaptomus appear to be functionally equivalent in their potential ability to control
ciliates.
705
C.W.Burns and M.Scfaallenberg
Keratella populations were unaffected by the presence of Daphnia and Boeckella in our study. Although Daphnia, particularly large Daphnia, can suppress rotifers, including several species of Keratella (Gilbert, 1988; Wickham and Gilbert,
1991), suppression is not always evident, either because some species of rotifers
have morphologies or behaviours that make them less susceptible to interference
(e.g. Gilbert, 1988), or possibly because rotifer data from field experiments can be
highly variable (e.g. Wickham and Gilbert, 1993). As Keratella abundances varied
greatly within treatments in our study, we cannot exclude the possibility of a Type
II error; it is worth noting, however, that the rotifer populations in Castle Lake,
California, were not suppressed by Daphnia or Diaptomus at densities of 15 I"1
(Brett et at, 1994).
The average turnover time of bacterial biomass in the enclosures in our study,
calculated from net growth rates, was ~8 days which is within the reported range of
several days to weeks for temperate lakes (Jlirgens and Glide, 1991, 1994). Bacterial abundance was positively correlated with chlorophyll a in enclosures without
added nutrients (n = 15, r = 0.644, P = 0.0095), which is consistent with the hypothesis that prod ucts of algal exudation and lysis provide the main source of energy for
bacterial production (Azam etai, 1983); small bacteria increased only in the nutrient-enriched enclosures in which algal biomass had increased markedly. These
observations support the hypothesis that bacterial growth in Lake Mahinerangi
was nutrient limited (bottom-up control). The increase in populations of large rods
over 4 days in the fertilized enclosures without added macrozooplankton is probably a result of selective grazing by ciliates and flagellates favouring an increase in
bacterial morphologies that are more resistant to protozoan grazing, and a poorer
ability of larger rods to compete with small single bacteria for substrates in the
unenriched enclosures (Glide, 1989), although substrate enhancement by the grazing activities of rotifers and small crustaceans (<150 |im) may also have stimulated
the growth of these rods (Arndt et ai, 1992; Peduzzi and Herndl, 1992).
Daphnia had strong negative effects on the density of large bacterial rods
(~2 n.m), but no measurable effects on the abundance of smaller rods and cocci
(<1 urn). Several authors report negative effects of Daphnia on bacterial populations in lakes (e.g. Riemann, 1985; Christoffersen et ai, 1990; Pace et al., 1990;
Jiirgens et al., 1994a; MarkoSovi and Jezek, 1993), but these are at higher daphniid
densities than in our experiments. Others report no effects of Daphnia on bacterial
abundance (Pace and Funke, 1991; Wickham and Gilbert, 1993; Brett etal., 1994).
Shifts in the morphometry of bacteria from large rods andfilamentsin the absence
of Daphnia to small cocci in the presence of Daphnia have been reported (e.g.
Glide, 1988; MarkoSova" and Jezek, 1993; Jurgens et al., 1994a). These shifts are
attributed to the less efficient retention by Daphnia of small bacteria compared to
larger cells (Brendelberger, 1985; DeMott, 1985; Glide, 1988; reviewed by Jurgens,
1994), and size-selective grazing by protozoans in the absence of Daphnia that
increase the proportion of grazer-resistant larger forms (Glide, 1988).
Boeckella had no effect on populations of large rods, probably because they
were too small for the copepod to collect. Thisfindingis consistent with well-documented inabilities, and inefficiencies, of calanoid copepods to collect small algae
and bacteria (Bogdan and Gilbert, 1984, 1987; Sanders et al., 1989; Pace et al.,
706
Microbial food web of a mesotropbic lake
1990), and their preferences for larger food particles (Vanderploeg, 1990). The
presence of Diaptomus had no effect on bacterial abundance in enclosures in
Castle Lake (Brett etal., 1994). When copepods dominated the macrozooplankton
in mesotrophic Schohsee, they caused an increase in bacterivorous protozoa which
grazed on small bacteria so that the bacterial assemblage consisted primarily of
large filamentous forms (Jlirgens et al., 1994a). The dramatic increase in small bacteria that occurred in the enriched enclosures in the presence of Boeckella was
associated with the decline in ciliate abundance in these enclosures due to boeckellid predation. The net growth rates of cocci and small rods in these enclosures were
strongly related inversely to ciliate densities (regression analysis on log-transformed data, n = 6; cocci: r2 = 0.877, P = 0.0058; small rods: r2 = 0.838, P = 0.0105).
These results are consistent with the regulation of small bacteria in these enclosures through bacterivory by ciliates (top-down control) (Sherr and Sherr, 1987;
Sanders et al., 1989; Christoffersen et al., 1990), although direct predatory control
of bacteria by ciliates in our study is unlikely because ciliate densities in Lake
Mahinerangi at the time of our study were too low (<5 ml"1) to have a significant
grazer impact. Even if they consumed bacteria at a rate of 420 bacteria day 1 ciliate"1, the estimated rate for ciliate bacterivory in Lake Vechten (Bloem and Ba'rGilissen, 1989), or at a rate of 15 120 bacteria day"1 ciliate-1, which is the maximum
rate measured by Sherr et al. (1989) for large marine ciliates, the ciliates in Lake
Mahinerangi could have removed only <1% to 7% of the bacterial biomass per
day.
If the enhanced bacterial biomass in enclosures containing copepods were an
outcome of reduced bacterivory by HNF, we might expect to find an inverse
relationship between the abundances of bacteria and HNF. Bacterial abundance
in the nutrient-enriched enclosures containing Boeckella was weakly correlated,
inversely, with the abundance of HNF (Spearman rank correlation, n = 6,
rs = -0.714, P = 0.110), which is consistent with predatory control of bacterial
populations by heterotrophic flagellates. Increased bacterial production in the
presence of macrozooplankton (cladocerans and copepods) has been reported
and attributed to stimulatory effects of nutrients released by the grazing activities
(sloppy feeding, excretion, defaecation) of the macrozooplankton (Crisman etal.,
1981; Peduzzi and Herndl, 1992). Monomeric carbohydrates released by marine
copepods enhanced the growth of bacteria, particularly in oligotrophic waters
(Peduzzi and Herndl, 1992). Although inorganic nutrients are unlikely to have
been limiting bacterial growth in the enriched enclosures, soluble substrates
released by Boeckella during feeding and excretion may also have stimulated bacterial growth in our experiments (bottom-up regulation).
The fact that the grazing effects of Daphnia on components of the microbial
food web were evident after 4 days and in the presence of added nutrients indicates
that top-down effects were stronger than nutrient effects in determining microorganism abundances in the presence of this zooplankter. The strong predatory
impact of Boeckella on ciliates occurred in the presence and absence of added
nutrients, indicating that ciliate populations were regulated more strongly by topdown control than by bottom-up effects; this conclusion is supported indirectly
by the lack of any positive correlations between the population growth rate, or
707
CW.Burns and M.Schallenberg
abundance, of ciliates and their potential food resources of bacteria and autotrophic picoplankton at both nutrient levels (Spearman rank correlations between
ciliate net growth rate and microorganism concentrations, all P > 0.2). Two factors
may have contributed to a lack of detectable changes in abundance or growth rates
of bacteria, picophytoplankton and flagellates in response to these predatorinduced depressions in ciliate biomass: (i) the potentially weak grazing impact of a
relatively low total ciliate abundance in Lake Mahinerangi and (ii) the incubation
period. Although 4 day incubations have been used in studies that are comparable
to ours (e.g. Elser and Goldman, 1991; Pace and Funke, 1991), a longer incubation
period may have resulted in detectable responses to changes in ciliate abundance.
The bacterial populations in Lake Mahinerangi, particularly those of large bacteria, are controlled from the bottom up by nutrients; large bacteria are also
strongly controlled from the top down by Daphnia, whereas small bacteria are
weakly controlled from the top down by HNF.
Model
The relative effects of Daphnia, Boeckella and inorganic nutrients on the microbial
community of Lake Mahinerangi are summarized in Figure 12. Inorganic nutrients
had strong stimulatory effects on the growth of phytoplankton, a large photosyntheticflagellateand large bacterial rods; weaker bottom-up effects were evident in
the growth of small bacteria, HNF and ciliates in response to increased resources.
In the presence of Boeckella, the top-down effects virtually ceased at the level of
ciliates. In contrast to Boeckella, Daphnia 'broke open' the microbial loop by feeding directly on ciliates,flagellatesand large bacteria, as well as on phytoplankton,
including some picoplankton. These contrasting effects of a cladoceran and a
Fig. 12. Effects of Daphnia, BoeckeUa and nutrients on the pelagic microbial food web of Lake Mahinerangi. Solid lines indicate top-down effects; broken lines indicate bottom-up effects. Increasing
strengths of the impacts are indicated by increasing thickness of arrows. Trophic and resource interactions that were not detected in this study have been omitted.
708
0.32
0.90
3.45
South Island
Lake Wakatipu
Lake Manapouri
Lake Mahinerangi
2007
50
640
5100
4020
980
Actual ciliates
(numbers I"1)
1920
3330
6860
2600
16 790
17 970
Predicted ciliates
(numbers \-')
19.2
29.3
2.6
37.7
30.4
22.4
(%)
Actual/predicted
C.W.Burns (unpublished)
C.W.Burns (unpublished)
This study
James el al. (1995)
Morrow (1995)
James et al. (1995)
Reference
•
*
Q-
|
2
I
veb of a mesotrophic
s
0.57
18.21
20.65
North Island
Lake Taupo
Lake Rotorua
Lake Okaro
Chlorophyll a
(M-gl1)
Table VIII. Concentrations of chlorophyll a and ciliates in the open waters of New Zealand lakes. Empirically determined ciliate densities are expressed as a
percentage of those predicted from chlorophyll a concentration according to the equation of Pace (1986): log Y = 3.547 + 0.538 log X, where Y is ciliate density
(numbers I"1) and X is chlorophyll a (p.g I"1). Data for North Island lakes are annual means based on 4-12 samples per lake
llcrobi
C.W.Burns and M.Sctiallenberg
copepod on the microbial food web of Lake Mahinerangi are consistent with predictions concerning the structures of microbial food webs in the presence and
absence of abundant Daphnia (Porter et al., 1988; Stocknerand Porter, 1988; Pace
et al., 1990; Wylie and Currie, 1991; Riemann and Christoffersen, 1993; Jurgens,
1994; Jurgens and Giide, 1994). If also consistent with hypotheses and models of
energy flow differences in £>ap/i«/a-dominated and copepod-dominated systems
(Scavia and Fahnenstiel, 1988; Wylie and Currie, 1991; Riemann and Christoffersen, 1993), they imply that in New Zealand's copepod-dominated lakes, more of
the carbon that is fixed in photosynthesis will be lost to heterotrophic respiration
(bacteria, flagellates, ciliates) and less will be available to higher trophic levels than
in the Z)fl/?/m/a-dominated lakes of the northern hemisphere.
By highlighting the relative importance of specific trophic linkages in the
microbial food web of a mestrophic lake, Figure 12 identifies some of the difficulties and limitations inherent in adopting too simplistic a view of energy flow in
microbial food webs as being controlled either by resources or by consumption
(top-down versus bottom-up). Figure 12 also illustrates the concurrent impacts of
both resource availability (bottom-up) and consumption (top-down) on the dominant alga and main components of the microbial food web. For example, the net
growth rate of Cyclotella responded strongly to nutrients (bottom-up), but was
equally strongly depressed by the grazing activities of Daphnia (top-down); the
total ciliate growth rate increased with increasing flagellate resources, and
decreased in response to predation by Daphnia and Boeckella, whereas bacterial
growth rates responded positively to increases in substrate concentration and
negatively to the grazing impacts of flagellates and Daphnia. The results of our
study provide empirical support for the finding of Gasol et al. (1995), based on
statistical analyses of the abundance of HNF in 16 Quebec lakes in relation to food
(bottom-up) and predation (top-down) variables, that both food (bacteria) and
predation (Daphnia) predicted HNF abundance reasonably well.
The distinctly different effects of a cladoceran and a calanoid on the microbial
community of Lake Mahinerangi prompt us to predict that in ecosystems that are
dominated by suspension-feeding calanoid copepods, either permanently, as in
some lakes and marine systems, or seasonally, as in many temperate lakes that do
not freeze, ciliate densities will be low relative to those that occur when calanoids
are less abundant. Calanoid copepods (Boeckella, Calamoecia), rather than Daphnia, tend to dominate the mesozooplankton of New Zealand lakes throughout the
year (Chapman and Green, 1987). Estimates of ciliate density are available for
only a few lakes in New Zealand, but in all of them ciliate densities are low relative
to those in temperate lakes of similar trophic state elsewhere (Table VIII). In light
of the strong top-down control of ciliates by Boeckella in our study, it is tempting to
speculate that calanoid dominance may contribute to low ciliate abundance in
New Zealand lakes.
Acknowledgements
This study was supported by grants from the Foundation for Research, Science and
Technology (grant number U0O313) and the University of Otago. We are grateful to Tim Dodgshun, Jane Kitson, Nigel Milton, Katrina Shierlaw, Rob Wass and
Andrew Winnington for help in the field and in the laboratory.
710
Microbial food web of a mesotrophic lake
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Received on June 6, 1995; accepted on December II, 1995
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