Download Microbial and classical food webs: A visit to a hypertrophic lake

MICROBIOLOGY
ECOLOGY
ELSEVIER
FEMS Microbiology
Ecology
17 (1995) 257-270
Microbial and classical food webs: A visit to a hypertrophic lake
R. Sommaruga
*
University of InnsbrucS Institute of Zoology and Limnology, Technikerstr. 25, A-6020 Innsbruck, Austria
Received 8 February
1995; revised 27 April 1995; accepted 9 May 1995
Abstract
Plankton
community
structure and fluxes of carbon for bacteria (production and bacterivory) were investigated in the
urban, hypertrophic Lake Rod6 (Uruguay) using a short time interval for sampling (5-15 d) during one year. The lake
sustains a high phytoplankton biomass (up to 335 pg I- ’ chlorophyll a) always dominated by the filamentous cyanobacteria
PZunktot/zrti agardhii. The zooplankton community was numerically dominated by rotifers and ciliates; cladocerans were
rare during most of the year. The rotifer abundance was very high (up to lo5 individual 1_ ’ ), the bacterivorous Anurueopsis
fissa being the most abundant species. Predation rates of heterotrophic nanoflagellates (HNF) on bacteria (range: 31-130
bacteria HNF-1 h- ‘) were higher than those reported in the literature for field studies. A carbon budget showed that HNF
can consume on average 91 and 76% of the bacterial carbon production in summer and winter, respectively. Bacterial
turnover times are the lowest reported until now from field conditions (5 to 42 h). Consequently, bacterial carbon production
was extremely high (72 to 1071 pg C 1-l d- ‘). Bacterial production was positively correlated to bacterial abundance but the
relationship was significantly improved by the inclusion of temperature (82% variability explained). My results support the
general trend for increased bacterial production with increasing trophic status, and suggest a lower energy transfer efficiency
to higher trophic levels in hypertrophic lakes due to the many trophic interactions involved.
Keywords: Planktonic
food web; Bacterial
production;
Bacterivory;
Carbon flow; Hypertrophic
1. Introduction
Hypertrophic lakes, the last stage in the trophic
state classification, are becoming common in several
parts of the world as a consequence
of increasing
water pollution [l]. Barica [2] has characterized hypertrophic lakes as shallow systems with high retention times, unbalanced nutrient and oxygen regimes,
extreme fluctuation
in nutrients, high productivity
and a relatively low abundance of zooplankton due
* Corresponding
author. Tel: +43 (512) 507-6121;
(512) 507-2930; E-mail: [email protected]
0168-6496/95/$09.50
0 1995 Federation
SSDI 0168-6496(95)00030-5
of European
Fax: +43
Microbiological
lake
to non-grazeable
filamentous phytoplankton. Studies
on plankton from those systems have been made less
frequently than in other lakes of different trophic
state [3-51. The microbial food web of hypertrophic
lakes has received little attention and information is
scarce, available only on a small number of systems
16-91.
Eutrophication
produces several direct and indirect structural changes in the pelagic food web,
notably to the phytoplankton
community [lo]. Although the abundance and biomass of the different
microbial components increases with increasing nutrient enrichment [11,12] the importance of the microbial loop in the C flux along the productivity
Societies. All rights reserved
2.58
R. Sommaruga / FEMS Microbiology Ecology I7 Cl995) 25 7-270
gradient compared to the “classical”
grazing food
chain (phytoplankton-zooplankton
link) is still uncertain. While Riemann et al. [13] supported the idea
that the importance of the microbial loop increases
with increasing nutrient loading, Weisse [14] stated
the opposite. Recently Weisse and Stockner [15]
reviewed this topic and argued that although microbial food webs dominate the carbon flow in oligatrophic systems they can be the most important
component
again under very eutrophic or hypertrophic conditions when Daphnia is absent. The role
of Daphnia for an efficient energy transfer from the
microbial food web to higher trophic levels has been
demonstrated
for mesotrophic and eutrophic lakes
[16,17]. The exclusion of Duphnia from the plankton
has been attributed to the dominance of colonial or
filamentous cyanobacteria in the phytoplankton community [18] or to a strong planktivory by fish [19]. In
lakes with low abundance of cladocerans the link
between picoplankton and macrozooplankton
is given
by flagellates, ciliates and rotifers but with a lower
energy transfer efficiency.
Based upon data collected over one year, this
paper presents the structure and dynamics of the
microbial food web components
in a hypertrophic
lake. To understand the carbon flow in the pelagic
system of this lake the structure of the phytoplankton
and zooplankton was investigated as well. Furthermore, the factors controlling bacterial production and
the predation impact of heterotrophic flagellates are
discussed in relation to previous models.
2. Material
and methods
2.1. Description
of the system and sampling strategy
Lake Rod6 situated in the city of Montevideo,
Uruguay (34”55’S, 56”lO’W) is small and shallow
(area = 1.3 ha, maximum depth = 1.1 m). There are
no limnological studies on this urban lake except the
knowledge of its evergreen water color and sporadic
observations .of phytoplankton.
Lake Rod6 has no
stream inputs but receives stormwater discharge from
an ill-defined urban area. Water overflows from the
lake via an intermittent
outlet only at high water
levels. The lake contains fish, principally
Cnesterodon decemmaculatus and Cichlasoma sp. Aquatic
macrophyte growth is sparse due to the shading from
the algal blooms but small pockets of Potumogeton
sp. occur.
Thirty-six samplings were made at the deepest
part of the lake from January 21 to December 28,
1992, at intervals of 5-15 d. The euphotic zone
corresponding to the first 50 cm of the water coIumn
was sampled with a 5 liter Schindler-Patalas
sampler.
Due to the existence of physical gradients in the first
centimeters of the water column, water was mixed 4
times before taking the subsamples always in the
same order. Sampling was carried out between 10:00
and 12:00 h. Bacterial production and bacterivory
experiments were made at the laboratory within 30
min after the samples were collected.
On each sampling date, water transparency, photosynthetically
active radiation,
temperature,
pH,
conductivity,
oxygen, total nitrogen and total phosphorus were measured to characterize the physical
and chemical conditions of the water-column.
2.2. Abundance
and biomass measurements
Chlorophyll
a was measured spectrophotometritally following extraction with hot ethanol [20]. Phytoplankton samples were preserved with acid Lugol’s
Iodine and enumerated using either a Sedwick-Rafter
chamber (for counting trichomes) or a sedimentation
chamber of 2-5 ml at 200 X magnification (for total
counts). In the former case, triplicate counts were
made. In the case of Planktothrix
400 trichomes
were measured at 200 x magnification
from a pool
made with all samples. Nauplii and rotifers were
counted together with ciliates in the sedimentation
chamber. When nauplii and rotifer numbers were
lower than 50 individuals, between 0.2 and 1.0 1 of
lake water was filtered through a 45 pm mesh
(Nytex, Switzerland) and then poured into a Bogorov
chamber and counted at 200 X magnification.
Rotifers were identified to the genus or species level on
live or fixed samples. Macrozooplankton
were collected with a Patalas trap, filtered through a nylon
mesh of 100 pm and fixed with sucrose-formalin
(final concentration
4%). The organisms
were
counted in a Bogorov chamber at 40 X magnification, and identified with appropriate keys.
Bacterial samples were fixed with formalin (final
concentration
2% v/v) and stained with the fluo-
R. Sommaruga / FEMS Microbiology Ecology 17 (1995) 257-270
259
rochrome DAPI [21]. More than 400 bacteria were
counted on black membrane
filters (Poretics 0.2
pm) at 1250 X magnification in a Nikon epifluorescence microscope with a BP 365, FT 395, and LP
397 filter set. The size of the bacteria was determined with an image analysis system as described in
Psenner [22]. Cell volumes were computed with the
following formula:
ments using appropriate geometric formulas. I used a
single conversion factor of 110 fg C pm-”
[26]
although changes in ciliate cell volume after fixation
with mercuric chloride are variable for different
species [27].
V=(w2x~/4)x(I-ww)+(~xw~/6)
Natural bacteria from the lake were grown in
sterile lake water supplemented
with a barley seed
and harvested during the log phase determined by
following the absorbance at 650 nm. Then the heatkilled bacteria were stained with 5-([4,6-dichlorotriazin-2-yl]amino)fluorescein
(DTAF)
according
to
Sherr et al. [28]. The fluorescently-labeled
bacteria
(FLB) had a mean length of 0.96 k 0.34 pm and a
mean width of 0.4 + 0.1 pm with an equivalent
mean cell volume of 0.104 pm3.
Grazing experiments were conducted on 18 of the
36 sampling dates. Experiments were done independently for flagellates and ciliates under in situ conditions. FLB at a concentration
of ca. 15% of the in
situ abundance of bacteria were added for ciliates
and ca. 25% for flagellates. Subsamples of 20 ml
were taken during 25 min at 3-5 min time intervals
and fixed with alkaline Lug01 (final concentration
0.5%), followed
by the immediate
addition
of
borate-buffered
formalin (final concentration
3%;
[29]). The samples were kept refrigerated (5°C) and
dark until analyses within 24 h. Preserved samples
were stained with DAPI, filtered onto 1 pm black
membrane filters (Poretics) and washed 3 times with
cold particle-free tap water. DAPI-stained organisms
were located under the epifluorescent microscope at
400 X (ciliates) and 1250 X (flagellates) under UV
light (365/395/397
nm) and FLB inside vacuoles
were counted using the blue-light filter set (450490/510/520
nm) at 1250 X magnification.
Flagellates were checked for the presence of plastids as
described above. Labeled food concentrations
were
estimated from counts of DTAF-stained
cells from
the to samples under blue excitation. The uptake rate
was estimated from a linear regression between time
and the mean number of FLB ingested per individual. Linear regressions with a r2 < 0.9 were not
included in the results. Flagellates without FLB ingestion were included in the calculation. Clearance
(1)
where V= volume ( ,cLm3), w = width ( pm) and
1 = length (pm). Accuracy of the algorithms used
was confirmed with independently
calibrated microspheres (Molecular Probes, USA) of known size (M.
Kriip bather pers. comm.). Biovolumes were transformed into biomass using an allometric relationship
[23] expressed in the formula:
c = 0.12 x v”.72
(2)
where: V= cell volume ( pm31 and C = carbon (pg
cell - ’ ).
The abundance of active (INT-reducing)
bacteria
was determined
according to Zimmermann
[24].
Glycerin was always used as the mounting medium.
Samples for counting HNF were treated in the
same way as described for bacteria. Each individual
was checked with a BP 490, FT 510, and LP 520
filter set for the presence of autofluorescence
i.e.
presence of plastids. Length and width of individuals
were measured at 1600 X magnification with a calibrated ocular micrometer and used to calculate the
volume assuming appropriate geometrical formulas.
The mean cell volume was used to estimate biomass
using a conversion factor of 220 fg C pump3 [25].
Ciliate samples were fixed immediately with 1 ml
of a saturated solution of HgCl, and enumerated
using the inverted microscope technique. Depending
on ciliate density, 5 to 10 ml aliquots were settled for
24 h and the entire surface of the settling chamber
was examined at 200 X . Two drops of Bromophenol
Blue (0.04% w/v) were added to help to differentiate the individuals.
Total counts always exceeded
100 individuals.
Ciliate biomass was estimated by
multiplying the abundance by mean cell volume in 3
different size classes: < 20 pm, 20-35 pm and
> 35 pm calculated from direct volume measure-
2.3. Bacterivory
ments
and bacterial
production
experi-
260
R. Sommaruga / FEMS Microbiology
rates (CR) were estimated
tion:
using the following
CR = UR/FLB
equa-
(3)
where: UR = uptake rate in (FLB ingested individual -’ h- ‘> and FLB = concentration of FLB nl- ‘.
The [ 14C]leucine method [30,31] was used to estimate bacterial production. [ I4C]Leucine (Amersham,
UK) of 310 mCi mmol-’ specific activity was added
to 3 vials containing
10 ml lake water at a final
concentration of 20 nM. Saturating concentrations of
Leucine were determined experimentally
by measuring incorporation
rates at various concentrations
of
substrate. Except for one occasion (December: 40
nM), saturation was reached at 20 nM. All samples
were corrected for abiotic incorporation by subtracting the radioactivity in formalin-killed
controls (2%
final concentration).
Protein was extracted in cold
trichloroacetic
acid (final concentration
5%). Filters
were washed with 80% cold ethanol [32]. The moles
of leucine incorporated per hour and carbon production were calculated using the formula developed by
Simon and Azam [31], assuming a 2-fold intracellular dilution. Cell production was estimated using the
estimated
empirical
conversion
factor. Bacterial
turnover times were computed as the ratio of bacterial abundance (cells 1-l ) and bacterial production
(cells 1-l h-l).
2.4. Empirical
conversion factor
An empirical
was estimated in
pling, 100 ml of
pressure through
conversion factor for [ 14Clleucine
November. Immediately after samlake water were filtered under low
a 1.0 pm pore size filter and mixed
Table 1
Salient physico-chemical
information
Ecology 17 (1995) 257-270
with 400 ml of the same water filtered through a 0.2
pm filter. Bacterial numbers and [14C]leucine incorporation were followed during 42 h at 20°C (annual
mean = 18.9”C) using the procedures
described
above. A conversion
factor of 12.9 X 1016 cells
mol-’ was derived using the approach of Ducklow
and Hill [33].
2.5. Carbon budget
The budget was made from estimated and calculated values averaged over the summer and winter
periods using the following conversions factors and
assumptions: Carbon phytoplankton biomass was estimated only for Planktothrix
using the formula
C = 0.11 X (V) [34]; biomass of Anuraeopsis fissa
-the most abundant bacterivorous rotifer -was calculated assuming a C content of 0.009 pg C individual-’ [35]; biomass of crustaceans was estimated
using the formula for species or pooled equations
described in Dumont et al. [36] and converted to
carbon assuming a C:dry weight ratio of 1:2; bacterial biomass were estimated using the allometric
approach Eq. 2. The amount of carbon ingested by
flagellates was calculated from community
uptake
rates converted into carbon units using the respective
mean bacterial cell volumes and Eq. 2. For Anuraeopsis fissa the same procedure was followed except that a mean ingestion rate (1283 bacterial individual-’ h- ‘) was derived from values given in
Ooms-Wilms [37] for summer experiments made in
Lake Loosdrecht (minimum: 1020 bacterial individmaximum:
1546
bacterial
ual -1 h-1.
individual-’
h- ‘).
of Lake Rod6
Parameter
Mean
Range
Temperature PC)
Oxygen saturation
18.9
105
8.4
552
0.20
0.53
0.43
2.90
8.5
8.2-28.0
50-170
8-9
400-740
0.15-0.30
0.50-0.60
0.16-1.0
1.10-4.7
1.6-15.0
(%)
PH
Conductivity ( &G cm-’ )
Transparency (m)
1% Photosynthetically
active radiation (m)
Total phosphorus (mg 1-l )
Total nitrogen (mg 1-l )
Total nitrogen: total phosphorus (by weight)
Values are from O-O.5 m of the water column (n = 36).
R. Sommaruga / FEMS Microbiology
Ecology 17 (1995) 257-270
261
2.6. Statistics
Correlations
among variables were made using
the non-parametric
Spearman rank test. Where necessary, the data were log,, transformed to equalize
the variance over the range of observations and to
meet the normality assumptions of least-squares regression analysis. Normality of the variables and
residual values from each regression were assessed
using the Kolmogorov-Smirnov
test. For multiple
standardized
partial regression coeffiregressions,
cients ( p coefficients) were calculated to provide an
indication of the impact of the residual unexplained
variance of each independent variable on the dependent variable.
300 n-
‘E
250 200 -
E
150 -
_m
100 -
6
50 ”
J
F
M
A
M
J
JASON0
MONTHS
3. Results
3.1. Physical
water-column
and chemical
characteristics
of the
Values for the main physical and chemical features of Lake Rode are presented in Table 1. Due to
the shallowness of the lake, the water-column
was
mixed most of the time. However, during the day in
summer it was stratified with a maximum difference
of 3°C between surface and 0.60 m. During the night
and depending on wind speed, the water-column was
completely mixed. The lake was well oxygenated
except during summer when a steep decrease in
oxygen concentration was observed with anoxic conditions at the bottom. The TN:TP ratio showed that
N might be the limiting nutrient most of the time.
3.2. Components of the classical food web: phytoplankton and zooplankton
Of 27 species of phytoplankton
found, the
cyanobacteria
Planktothr~
agardhii dominated all
year around representing between 82 and 99% of the
total abundance of phytoplankton. Euglenales, mainly
Euglena, Trachelomonas and Phacus, were the second most abundant taxonomic group. A complete list
of phytoplankton species is available from the author
upon request. The mean number of trichomes of P.
agardhii was 4.2 X lo7 1-l. The minimum biovolume was observed in winter (3 X 10” pm3 1-l) and
Fig. 1. Temporal development of Planktozhrir biovolume (a) and
chlorophyll a (b) in the first 50 cm of the water-column of Lake
Rod&
the maximum in summer (1.5 X 1011 pm3 1-r; Fig.
la). The mean chlorophyll a value was 223 mg me3
with a minimum value of 99 mg me3 in autumn and
a maximum of 335 mg m -’ in summer (Fig. lb). A
positive correlation was found between the abundance of P. agardhii and chlorophyll a (rs = 0.527,
P < 0.001).
Due to space restriction figures are shown only
for the main taxa. The Calanoida (Fig. 2g) were
represented by one species, Notodiaptomus incompositus, with abundances ranging from 0.1 to 23.5
individuals
1- ’ for adults and from 0.1 to 44.0
individuals
I- ’ for copepodites.
Maximum abundances of both adults and copepodites were observed
at the end of fall and in spring. The most abundant
cyclopoid
copepod
was Tropocyclops
prasinus
meridionalis, ranging from 1 to 53 individuals 1-l
for adults and 0.3 to 31 individuals 1-l for copepodites (Fig. 2h). Copepods, both adults and copepodites, were very often observed to be colonized by
the peritrichous ciliate Epistylis sp. Nauplii were
very abundant (Fig. 2f) with densities between 50
and 11800 individuals
1-l. Maximum abundance
was observed in spring. Cladocerans (Fig. 2i) were
represented by three species of which Moina micrura was the most abundant with a maximum den-
R. Sommaruga / FEMS Microbiology Ecology 17 (19951257-270
262
600
400
_
200
'i
8
6
a8
.E
4
0
:
Ciliates > 35 pm
0)
::
S
40
iii
20
0
a
200
5
100
i
0
/
ri
.+._%_A&,
12008
8000
i
Nauplii
A
Calanoid copepods
200
~-~-
Cladbcerans
100
I
0
b
----~-.
_
-*--
L..
JFMAMJJASONO
MONTHS
Fig. 2. Changes in abundance (0) and biomass (0) of components of the plankton in the first 50 cm of the water-column
in
Lake Rod6
sity of 194 individuals 1-l. Both Daphnia parvula
and Diaphanosoma birgei were present at low abundances (< 3 individuals
1-l). All three species
reached their maximum abundance in spring, disappearing by December. Rotifers were the most abundant group of metazooplankton
with densities between 1200 and 129600 individuals 1-l (Fig. 2e).
The most abundant rotifer was Anuraeopsis
spp.
mainly A. fissa who reached a maximum of 123 200
individuals 1- ’ at the end of the summer.
3.3. Components
of the microbial food web
The abundance of HNF ranged between 1.1 X lo6
and 3.0 X 10’ 1-l with a mean abundance of 1.2 X
10’ 1-l (Fig. 2a). HNF density reached the maximum at the beginning of fall and the minimum in
winter. The size of HNF ranged between 2 and 10
pm length. Biomass ranged between 8.4 and 579 pg
C 1-l with a mean value of 129 pg C 1-l (Fig. 2a).
Maximum biomass was observed in summer and
minimum in winter (Fig. 2a). HNF abundance was
correlated with the bacterial abundance (r, = 0.518,
P < 0.01, n = 36).
The mean abundance of ciliates was 31700 individuals 1- ’ with a minimum of 3600 and a maximum of 84 000 individuals 1-l. Ciliates in the size
class from 20 to 35 pm were the most abundant with
densities ranging from 1300 to 68 600 individuals
1-l (Fig. 2~). Dominant species in this size class
were Halteria sp., Askenasia sp. and Strobilidium
sp. High abundances
were observed in summer
(February) and spring (October) while the lowest
occurred in winter (July). Ciliates in the size class
< 20 pm were numerous only in summer with a
maximum abundance of 27 000 individuals l- ’ (Fig.
2b) and dominated by Urotricha sp. Ciliates > 35
pm were abundant at the end of summer, in winter
and in spring (Fig. 2d) but present in lower densities
(O-24 200 individuals l-‘). Taxa representing
this
size class were Coleps hirtus, Vorticella
sp.,
Paradileptus sp., Frontonia sp., and Didinium spp.
Maximum abundance at the end of the summer was
made by Vorticella sp. and Didinium spp. The winter increase in numbers was due to Paradileptus sp.
which together with Frontonia, Didinium spp. and a
Paramecium
type were responsible for the spring
peak in abundance.
Total ciliate biomass ranged
from 4.3 to 288 pg C 1-l. With the exception of
January when ciliates < 20 pm contributed 33% to
the total biomass, the main contribution during the
rest of the year was made by the larger size classes
(Fig. 2b-d).
Bacterial abundance ranged from 1.5 X lo9 1-l
to 2.0 X 10” I-’ with a mean of 7 X lo9 1-l (Fig.
3a). Summer values were an order of magnitude
higher than winter values. More than 95% of the
bacteria were free-living. Mean cell volumes (MCV)
ranged from 0.065 to 0.546 pm3. Mean cell volume
was inversely
correlated
to temperature
(r, =
- 0.865, P < 0.001, n = 30). Biomass values ranged
from 80.2 to 443 pug C 1-l (Fig. 3a). Very long
bacteria of up to 210 pm length accounted for
4-16%
of bacterial abundance.
A more detailed
study of these bacteria larger than their predators
will be published elsewhere. The number of INT-reducing bacteria oscillated between 0.4 and 6 X lo9
1-l accounting for 16.5-100% of the total bacterial
R. Sommaruga / FEMS Microbiology Ecology I7 (1995) 257-270
263
abundance (Fig. 3b). Interestingly,
autotrophic picoplankton was not found in Lake Rod6 and therefore heterotrophic bacteria are the only food source
in the picoplankton size range.
3.4. Bacterial
$/Q?/dLyq
secondary production
The [‘4C]leucine
incorporation
follows a very
clear seasonal pattern with the maximum value in
summer (14.4 nmol 1-i h-i) and minimum in winter
(1.1 nmol 1-i h- ‘). Accordingly,
bacterial carbon
production ranged from 72 to 1071 pug C 1-l d-’
with a mean of 587 ,ug C 1-i d- ’ (Fig. 3~). Temperature was positively correlated with leucine incorporation
rates (r, = 0.900,
P < 0.001,
n = 36).
Turnover times were extremely fast and highly variable (5-42 h; Fig. 3d).
3.5. Bacteriuory
by protists
JFMAMJJASOND
MONTHS
Fig. 3. Temporal
development of bacterial abundance and biomass
and percentage
of INT-reducing
bacteria (b),
bacterial carbon production (c) and turnover time (d) in the first
50 cm of the water-column in Lake Rod&
(a), abundance
Table 2
Summary
Date
of estimated
uptake and clearance
Uptake rate
(bacteria HNF-’
h- i)
rates by heterotrophic
A summary of estimated grazing parameters is
shown in Table 2. Uptake rates by HNF ranged from
31 to 130 bacteria HNF-’ h-’ with higher values in
summer. Corresponding clearance rates (3.7 to 29 nl
HNF-’ hh’) were higher in winter and inversely
nanoflagellates
(HNFI, January
29-December
28, 1992 in Lake Rod6
Clearance rate
(nl HNF-’ h-i)
Water column
cleared dd’ (%I
Bacterial cell production
consumed (%I
Jan 29
Feb 12
Feb 19
Mar 19
Apr 02
May 08
May 28
Jun 25
JuI 24
Aug 20
Sep 10
Sep 24
Ott 15
Ott 27
Nov 12
Dee 01
Dee 14
Dee 28
82
39
40
104
42
38
38
34
59
40
31
58
60
40
59
112
121
130
5.4
3.7
5.1
22.1
5.1
13.9
12.9
22.5
28.9
13.2
19.4
11.5
8.9
7.8
4.8
9.2
10.3
17.6
269
95
199
415
110
289
196
131
164
252
550
245
148
531
178
294
440
624
95
35
42
53
51
31
75
19
79
122
174
61
44
100
106
112
116
107
Mean
63
12.3
285
79
264
R. Sommaruga / FEMS Microbiology
correlated to temperature (r, = - 0.529, P < 0.05).
The percentage of the bacterial standing stock removed per day was very high with values equivalent
to 625% of the standing stock. Community uptake
rates were correlated with the abundance of bacteria
and temperature (I, = 0.794 and 0.781 respectively,
P < 0.001). When predation impact by HNF was
compared to the bacterial production the percentage
consumed ranged from 19 to 174.
Predation experiments with ciliates were not successful. In some cases, FLB were observed inside
vacuoles but uptake was highly variable, making
estimations impossible. The rotifer Anurueopsis was
observed with FLB as well as with pigments (autofluorescence) inside.
4. Discussion
4.1.
The
dominance
and its consequence
of filamentous
cyanobacteria
for the zooplankton
When lakes change from mesotrophic to eutrophic
or hypertrophic conditions the diversity of the phytoplankton
community
decreases [38]. During this
trophic shift, cyanobacteria become dominant in the
phytoplankton
assemblage both in terms of abundance and biomass. In some cyanobacterial
lakes,
Planktothrix agardhii (formerly Oscillatoria) has become dominant over the green algae, diatoms and
N,-fixing cyanobacteria
[39]. Virtual monocultures
of this species are typical for the most hypertrophic
phase of a lake and described as a ‘climax species’
with a peak in abundance in autumn and summer
[40]. However, under some conditions,
it can be
found the whole year round [41]. This is the case in
Lake Rod6 where P. agardhii is the dominant phytoplankton
species representing
always more than
82% of the total abundance.
P. agardhii has an
extremely effective light-capturing mechanism, chromatic adaptation, a low energy requirement for maintenance and a particularly efficient transfer of photosynthetically-fixed
carbon to growth under lowirradiance levels [3]. Zevenboom and Mur [38] have
proposed a hypothetical
model to explain phytoplankton succession in lakes of increasing P-loading.
The model shows conditions under which P. agardhii becomes favored, notably an increase in self
Ecology 17 (1995) 257-270
shading, a lower a,,/~,,, ratio, a lower light-energy
availability and N-limiting conditions. Light is limiting in Lake Rod6 as the euphotic zone is restricted to
ca. 0.5 m and for most of the time (except during
day in summer) the water column is totally mixed
and therefore the z,,/z,
ratio is low. Optimum
growth conditions of this species - both in cultures
and in lakes -are observed when the N:P ratio is 5-9
[41]. Forsberg et al. [42] have reported that TN:TP
values < 10 are N-limiting,
> 17 are P-limiting, and
ratios between 10 and 17 may be either N-or P-limiting or both. In Lake Rod& TN:TP ratios show that N
is the primary limiting nutrient (Table 1) and that
maximum abundance of Planktothrix occurred at the
time when N deficiency was very strong (TN:TP
value ca. 4).
An important consequence for the planktonic food
web structure of Lake Rod6 is the inability of zooplankton to graze trichomes of Plunktothrix (> 100
pm long). Although the proportion of other phytoplankters is small their absolute abundance (1.3 X
lo’--4.2 X lo6 I-’ represents an important food
source. However, this resource may not be fully
available
due to the mechanical
interference
of
Planktothrix for zooplankton
grazers. Experimental
and field results indicate that high concentrations of
filamentous algae affect the nutrition of herbivorous
zooplankton [43] and reduce drastically the reproduction and growth rates of cladocerans [18]. A noticeable characteristic of the zooplankton community of
Lake Rod6 is the absence of cladocerans for most
time of the year with only a short peak in spring,
mainly made by Moina micrura. Infante [43] suggested that a long period of absence of Moina
micrura, Ceriodaphnia and Diaphanosoma
in Lake
Valencia (Venezuela) may have been caused primarily by the presence of high abundances of cyanobacteria like Oscillatoria and Lyngbya. While this argument may hold for most part of the year in Lake
Rod& the drastic disappearance
of cladocerans in
December can not be attributed solely to the interference of Planktothrix as abundance of trichomes in
October and December were not markedly different.
A possible explanation may be the fact that from
December to March schools of the planktivorous fish
Cnesterodon
decemmaculatus
(Poeciliidae,
Cyprinodontiformes;
adult size 3 cm) were observed and
captured inside the water sampler (up to 10 individu-
R.Sommaruga/FEMSMicrobiologyEcology
17(1995)
257-270
als). The impact may be enhanced in summer when
owing to low oxygen concentrations
at depth zooplankton distribution is mostly restricted to the upper
0.5 m of the water column, making them more
vulnerable for fish predation. In brief, the crustacean
zooplankton community of Lake Rod6 is subjected
to a particularly harsh form of trophic interactions
caused by a heavy predation pressure from planktivores and the dominance of non-edible algae. Rotifers became dominant among the metazooplankton
and bacterivorous
species like Anuraeopsis fissa
reach very high abundance (10’ individuals l- ‘).
4.2. A highly dynamic microbial food web with several trophic interactions
In addition to rotifers, the ciliate assemblage also
dominated the zooplankton in terms of abundance.
As well as rotifers, ciliates of all three size classes
reached the highest abundance in summer, declining
later in winter and showing the clear effect of temperature on their seasonal dynamics. The abundance
found in Lake Rod6 was below the range of 90000215 000 individuals
l- ’ found for a set of hypertrophic lakes in Florida with chlorophyll
a values
> 56 mg me3 [lo]. The mean annual abundance in
Lake Rod6 was 32000 individuals 1-r and the maximum 84000 individuals 1-l. A possible explanation
for this discrepancy could be a high predation pressure on the ciliate community by the zooplankton
community
as was found in several studies and
summarized
by Gifford [44]. Some indications
of
possible predator-prey
interactions
among rotifers
and the smaller ciliates of different size classes are
clearly visible at the end of February and in October
(Fig. 2). Didinium is a taxon well known to feed on
other ciliates.
In Lake Rod6, the seasonal oscillation of HNF
abundance was very pronounced
changing by one
order of magnitude between winter and summer (Fig.
2a). Compared to Priest Pot (England),
a hypertrophic system but with lower phytoplankton biomass
(range Chlorophyll
a: 32-41 mg rnp3 [12]) mean
abundance of HNF in Lake Rod6 was lower (4.3 X
lo7 individuals 1-r and 1.7 X lo7 individuals l-‘,
respectively). However, HNF biomass reached very
high values of up to 579 pg C 1-r although the
means calculated with the same conversion factor
265
were similar (Lake Rod& 129 and Priest Pot: 118
pg C I-‘). As shown above, it seems that a high
predation pressure at this trophic level is exerted by
ciliates. A reduction in predation pressure on HNF
by nanociliates and ciliates in the size class 20-35
pm when they were concurrently
preyed upon by
large ciliates and possibly larger zooplankton can be
observed in March and October (Fig. 2). Berninger
[12] has argued that in productive systems the increased predation pressure keeps prey populations
well below the carrying capacity, and my results
support this idea.
HNF were the main consumers of bacterial standing stock (95-625%
removed per day) with very
high individual uptake rates of up to 130 bacteria
HNF-i hh’. The last value is similar to those found
in experiments with cultures [45] and 17-times higher
than the average uptake rate for HNF found in
freshwaters studies [46]. Such extreme values (>
100%) have also been found by others [47]. However, this calculation gives only a rough idea or
probably a wrong figure of the bacterivory impact
because clearance rates [48] as well as HNF and
bacterial abundances [49] differ significantly during
the day. Therefore, an extrapolation
of one value
from a finite time measurement to 24 h can lead to
under or overestimates
depending on the time the
bacterivory experiments were done. A comparison to
bacterial production is more appropriate and with the
exception of one value (174%), the percentage of
bacterial production consumed in Lake Rod6 was
close to or under 100%. A very important point to
understand the overall impact of the HNF on bacteria
is the existence of very long bacterial cells that
escape to predation. Therefore, the high values of
predation impact found in Lake Rod6 do not necessarily imply a collapse of the bacterial assemblage. I
have also used the model developed by Vaqut et al.
[46] to estimate total grazing rates (their GT) of the
community (including organisms other than HNF).
This model uses temperature and the abundance of
HNF and bacteria as independent variables and explain 53% of the variability of GT (data set for the
whole temperature range: 1.5-32°C).
Using mean
values of these variables for Lake Rod6 (18.9”C,
11749 HNF ml-’ and 6.9 X lo6 bacteria ml-‘) the
model predicts a lower value (log GT = 5.1) than
observed (5.9). The difference may be due to other
266
R. Sommaruga /FEMS Microbiology Ecology 17 (19951257-270
factors accounting for the variability
included in the model.
4.3. Factors
production
controlling
bacterial
of GT and not
abundance
and
106
Bacterioplankton
production and abundance have
typically been compared with primary production,
chlorophyll a, extracellular organic carbon production, and other variables in an attempt to demonstrate
how growth is regulated in situ. Bird and Kalff [50]
have found chlorophyll a to be correlated with bacterial abundance along a trophic gradient. Cole et al.
[51] have presented bottom-up (resource control) regressions relating bacterial production to chlorophyll
a and primary production for marine and freshwater
systems of different trophy. However, these studies
did not include systems with chlorophyll values >
200 mg me3. Introducing new data from systems of
higher trophy may help to evaluate the generalization
of previous models. In Lake Rod6 bacterial abundance was significantly
correlated to chlorophyll a
(r, = 0.55, P < 0.01) but the use of the mean chlorophyll value (223 mg mP3) to predict the number of
bacteria with the equations of Bird and Kalff [50]
and Cole et al. [51] (5.6 X 10’ and 1.7 X lo7 ml-‘,
respectively) gave higher values than the observed
mean (6.9 X lo6 bacteria ml- ‘). Although more data
in the upper chlorophyll range are needed, my results
and those from Robarts and Wicks [8] indicate that
there is a decline in bacterial numbers relative to
chlorophyll concentration along the trophic gradient.
Bird and Kalff [50] suggested that this may be a
necessary consequence
if bacterial productivity per
unit bacterial biomass increases at a faster rate with
increasing trophic status than primary production per
unit chlorophyll. However, Robarts and Wicks [8]
did not support this idea as they found in hypertrophic Hartbeespoort
Dam (South Africa) a very
low bacterial
production
(maximum
46 pg C
1-l d- ‘> although chlorophyll and primary production are the highest recorded in the literature ( > 6500
mg mm3 and 8886 mg C mm3 h-‘, respectively).
Conversely, my results indicate that there is an increase in bacterial production with increasing trophy
although the model of Cole et al. [51] underestimate
the observed values. In Lake Rod6 bacterial production is very high with a mean value of 587 pg C
10’
BACTERIAL
104
Planktothrix
ABUNDANCE
2.104 3.104
ABUNDANCE
(cells ml -1)
5.104 7.104
(thricomes
105
ml
-1)
Fig. 4. Bottom-up correlations
in Lake Rod6 between leucine
incorporation and bacterial abundance (a) and Planktothrti abundance (b).
1-l d&’ and a maximum of 1071 pg C 1-l d-l well
above the highest value registered (302 pg C
1~’ d- ‘> in a survey of 275 data from 22 freshwater
systems [52]. This corresponds well to the rapid
bacterial turnover times (5-42 h) and the high percentage of active bacteria registered (16-100%).
Moreover, considering the number of INT reducing
bacteria instead of the total number, the turnover
times will be in some cases even faster. The incorporation of leucine was significantly
correlated with
bacterial abundances as well as with Planktothrix
abundances (Fig. 4a and b).
A possible explanation to understand the contradictory findings in Lake Rod6 and Harbeespoort
Dam may be differences in phytoplankton
species
dominance.
In Hartbeespoort
Dam
Microcystis
aeruginosa is the dominant autotroph producing very
dense scums in the top meters. Although one would
expect a high substrate supply from this high autotrophic biomass Robarts and Zohary [53] have
argued that bacteria were substrate limited, based on
enrichment experiments and cell size. In fact the size
of bacteria was very small with a MCV = 0.013
Frn3 [8]. Beside the arguments on substrate limitation there is also some evidence that the toxin produced by Microcystis aeruginosa affects the survival
of bacteria and flagellates [54] as well as bacterivory
rates (Sommaruga et al., unpublished). Although Ro-
R. Sommaruga / FEMS Microbiology
barts and Wicks [8] did not reported abundance or
uptake rates of HNF they assumed that flagellate
bacterivory was low.
Another important factor to explain variability in
bacterial production within and among systems is
temperature. The role of temperature on laboratory
bacterial cultures is well known. Recently, Shiah and
Duklow [55] found temperature to be the most important factor regulating bacterial production, abundance and growth rate in Chesapeake Bay. Furthermore, Pomeroy and Wiebe [S6] have stressed the
important role of temperature as a main controller of
bacterial growth in aquatic systems. Also, temperature is an important modulator of the bacterial cell
size. Hagstriim and Larsson [57] found that at a
constant bacterial growth rate higher temperatures
produce smaller cells. The analysis of the relationship between bacterial production
and abundance
was significantly improved by the inclusion of in situ
temperature as an additional independent
variable.
The following equation was found for Lake Rod&
1ogBP = 0.37 + 0.16 log NB + 0.042T
(n=36,
r* = 0.816)
(4)
where BP = bacterial production ( ,ug C 1-l dd’);
NB = number
of bacteria (cells 1-l ) and T =
temperature CC>.
White et al. [52] have also found a better prediction level of bacterial production when temperature
was included in their freshwater data analysis. The
variability
explained by the independent
variables
was 2-times higher in Lake Rod6 than that found by
White et al. [52] ( r2 = 0.37). The standardized re-
Table 3
Major carbon pools for the planktonic
Lake Rod6
community
and fluxes of bacterial
gression coefficients for Lake Rod6 indicate that the
impact of temperature on production is greater than
that of abundance (/3 = 0.805 and 0.035, respectively). White et al. [52] have also found a greater
impact of temperature on bacterial production with
the exception of marine data where the reverse was
true. The inclusion of chlorophyll and Planktothrti
abundance in the case of Lake Rod6 as substitutive
or additional parameters did not improve the percentage of variability explained. Also the replacement of
the number of bacteria by the number of active
(INT) bacteria did not increase the variability explained. The results indicate that temperature is an
important positive modulator of bacterial production
on a seasonal as well as probably on shorter timescales and support the findings of White et al. [52]
for freshwaters.
4.4. Carbon flow in the euphotic zone
The carbon budget is far from being complete and
the number of assumptions make it far from perfect.
I am especially aware of the consequences in extrapolating production or bacterivory results from one
hour to one day. Nevertheless, the budgets for summer and winter illustrates relevant features from the
system (Table 3). In summer, HNF are able to crop
91% of the BP per day and have a biomass almost
equivalent to the bacteria. This implies a rapid bacterial growth to supply the amount of C required by
the HNF. The carbon pool of macrozooplankton
is
very much reduced compared to other highly eutrophic lakes like Frederiksborg Slotsso (715-1206
carbon production
Summer
Planktothrix
Bacteria
Flagellates
Ciliates
Anuraeopsis
Macrozooplankton
Values in brackets represent
a n.d., not determined.
267
Ecology 17 (1995) 257-270
and bacterivory
during summer and winter in
Winter
Pool
(/.LgCI_‘)
Flux
(FgCl-‘d-l)
Pool
(pgC1-1)
Flux
(PgCl-‘d-l)
13700
240
220
81
246
56
n.d. a
950
865 (91%)
n.d.
20 (2%)
n.d.
5000
1.51
29
40
8
26
n.d.
148
113 (76%)
n.d.
2.2 (1.5%)
the percentage
of bacterial
carbon production
consumed.
md.
See Material and methods for explanations.
268
R. Sommaruga / FEMS Microbiology Ecology 17 (1995) 257-270
pg c I-‘, [71) as a consequence of the suspected
heavy fish predation and poor food availability (inedible phytoplankton).
The rotifer pool, here only
exemplified by its most abundant species Anuraeopsis, dominated the rnetazooplankton
community not
only in abundance but also in biomass. However,
their estimated grazing impact on bacteria at maximum abundance accounts only for 2% of the BP
compared to 91% consumed by HNF. The 7% of BP
left in summer may be consumed by ciliates or lost
by other pathways (e.g. viral Iysis). In winter, all the
pools were reduced and the bacteria:HNF
biomass
ratio was 5:l. Nevertheless, in this period the HNF
crop 76% of the BP per day while Anuraeopsis
consumes only 1.5%.
The scenarios depicted here indicate that the
channeling of energy from the primary producers to
higher trophic levels through the ‘classical food web’
is reduced in this hypertrophic lake. Conversely, the
microbial food web is the main component for conveying energy to higher trophic levels although probably less efficiently due to the higher number of
steps involved and consequent energy losses. Also
the absence of keystone species like Daphnia able to
graze efficiently on preys of very different size leads
to energy sink rather than transfer. The data here
presented indicate a highly dynamic and active microbial food web supporting the ideas of Riemann
[13] and Weisse and Stockner [15]. The results gathered from this study enlarge our knowledge about
food webs in systems stressed by nutrient enrichment.
Acknowledgements
I thank Roland Psenner, Cohn Reynolds, John
Stockner and two anonymous
reviewers for comments made on a earlier version of the manuscript. I
am grateful to Lizet deLe6n, Daniel Fabisn, Daniel
Conde and Ma. Laura Arin for helping during sampling and plankton counting and to Eugen Rott for
the determination
of Planktothrix.
This work was
supported by a grant from CSIC Univ. de la
RepGblica (Uruguay), the North-South Dialogue Programme (Austria) and the Tonolli Foundation @IL).
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