Download and high-diversity planktonic food webs

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Structural and functional properties
of low- and high-diversity planktonic
food webs
URSULA GAEDKE* AND NORBERT KAMJUNKE
UNIVERSITY OF POTSDAM, INSTITUTE OF BIOCHEMISTRY AND BIOLOGY, MAULBEERALLEE 2, D-14469 POTSDAM, GERMANY
*CORRESPONDING AUTHOR: [email protected]
Received November 7, 2005; accepted in principle February 22, 2006; accepted for publication April 6, 2006; published online April 12, 2006
Communicating editor: K.J. Flynn
To test the consequences of decreased diversity and exclusion of keystone species, we compared the
planktonic food webs in two acidic (pH3), species-poor mining lakes with those in two speciesrich, neutral lakes. The ratio of heterotrophic to autotrophic biomass (H/A) was similar in acidic
and neutral lakes with comparable productivity. However, food webs in both acidic lakes were
largely restricted to two trophic levels in contrast to the four levels found in neutral lakes. This
restriction in food chain length was attributed to the absence of efficient secondary consumers, rather
than to productivity or lake size which resulted in unusually low predator–prey weight ratios, with
small top predators hardly exceeding their prey in size. In contrast to the neutral lakes, plankton
biomass size spectra of acidic lakes were discontinuous due to a lack of major functional groups. The
unique size-dependence of feeding modes in pelagic food webs, with bacteria in the smallest size
classes followed by autotrophs, herbivores and carnivores, was maintained for bacteria but the other
feeding modes strongly overlapped in size. Thus, their characteristic succession along the size gradient
was roughly preserved under extreme conditions but the flow of energy along the size gradient was
truncated in the acidic lakes. For most but not all attributes studied, differences were larger between
acidic and neutral lakes than between neutral lakes of different trophic state.
INTRODUCTION
Natural and anthropogenic stressors often decrease the
taxonomic, functional and trophic diversity of communities with far reaching but still poorly understood consequences for food web structure and function (Duffy,
2002; Hooper et al., 2005). Under extreme conditions
species number is typically low, and important functional
groups or typical keystone species including top predators may be lacking, leading to simply structured food
webs. This was found for sulphurous (Gasol et al., 1991),
saline (Wurtsbaugh, 1992), Antarctic (Laybourn-Parry,
1997) and acidic lakes (Kamjunke et al., 2004). This
study compares various attributes of the structure and
function of multi-trophic level planktonic food webs in
two extreme (acidic) lakes with those of two more typical
(neutral) lakes to test the effects of low diversity and
species exclusion on food web properties.
The planktonic food webs of the acidic lakes (Lakes
111 and 117, Eastern Germany) consist mainly of bacteria, two mixotrophic flagellate species, a few protozoan
and rotifer species and one (rare) crustacean species
(Chydorus sp.) which is found in the less acidic of the two
lakes (Wollmann et al., 2000; Kamjunke et al., 2004).
Other crustaceans (and fish) acting as keystone elements
in planktonic food webs are excluded by the adverse
environmental conditions. In contrast, the plankton composition of the neutral lakes (oligo-mesotrophic Lake
Constance and highly eutrophic Lake Müggelsee) covers
the full range of freshwater plankton from bacteria, small
and large phytoplankton and protozoans (mainly heterotrophic nanoflagellates and ciliates) to metazooplankton
(rotifers, cladocerans and copepods) (Arndt et al., 1993;
Gaedke et al., 2002, 2004). This allowed us to compare
species-rich and species-poor plankton food webs with
doi:10.1093/plankt/fbl003, available online at www.plankt.oxfordjournals.org
Ó The Author 2006. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
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and without larger metazoan grazers and to relate their
potential differences to the well-studied impact of trophic
state on food web properties. Given that microorganisms
were less affected by the extreme environment than
metazoans, we predict that food web traits dominated
by microorganisms such as bacterial and primary production are less altered than metazoan dominated traits,
such as consumer composition, top-down control by
higher trophic levels, predator–prey weight ratios and
food chain length.
Without major disturbances, pelagic food webs are
characterized by a continuum of organisms along the
size gradient (Sheldon et al., 1972; Gaedke, 1992), a
restriction of autotrophs to small size classes and predators that exceed their prey in size (Hairston and
Hairston, 1993). These properties lead to the characteristic succession of feeding modes (osmotrophy, autotrophy, bacterivory, herbivory and carnivory) from small to
large organisms, which distinguishes pelagic food webs
from terrestrial ones. They imply that body size provides
a simple integrative measure of organism niche. Thus,
major changes in trophic structure, keystone species,
food chain length and diversity were reflected in the
shape and size range covered by the biomass size distribution (Tittel et al., 1998; Gaedke et al., 2004). We use
biomass size spectra to provide insight into the functional
diversity of the plankton communities, the flux of matter
and energy along the size gradient and explanations for
biomass accumulations in certain size ranges (Platt and
Denman, 1978; Borgman, 1982; Gaedke, 1993). They
are also used to determine to what extent a remarkable
feature of pelagic food webs (i.e. the continuous succession of feeding modes along a size gradient) is preserved
under extreme conditions. For the larger sized organisms, we predict major deviations between biomass size
spectra of acidic and neutral lakes in respect to biomass
distribution and the succession of feeding modes.
To analyse potential deviations in basic food web
properties between species-rich and species-poor food
webs in common and extreme environments and to test
the above-mentioned predictions in particular, we quantified and compared among lakes:
(i)
(ii)
(iii)
the bacterial and autotrophic biomass, production
and turn-over rates forming the energetic basis of
the food webs;
the functional composition of each of the plankton
communities to provide insight into the quantitative importance of major functional groups and the
ratio of heterotrophic and autotrophic biomass
(H/A);
the trophic structure, using the distribution of biomass across the different trophic levels (i.e. trophic
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biomass pyramids), and food chain length, to elucidate major energy flux patterns and
taxonomically resolved biomass size spectra, the
size spectra of the different modes of nutrition
and predator–prey weight ratios.
METHODS
Study sites
For the comparison, we selected two acidic and two neutral lakes. Lakes 111 and 117 are acidic, brown coalmining lakes situated in Eastern Germany (Lusatia;
518290 N, 138380 E). Iron sulphide oxidation in the soils
decreased the pH in the mining lakes (pH 2–4), which
are buffered by ferric iron hydroxide (Geller et al., 1998).
Another characteristic of some lakes (e.g. Lake 111)
is the red–brown colouration of the water caused by
extremely high concentrations of dissolved ferric iron
(150 mg Fe L–1). The two acidic lakes are relatively
small (Table I). The planktonic food web of the moreacidic lake (111, pH 2.6) consisted mainly of single-celled
and filamentous bacteria, the two mixotrophic flagellates
Chlamydomonas acidophila and Ochromonas sp. and Heliozoa
as top predators. Very few rotifers (Elosa worallii and
Cephalodella hoodi), ciliate and rhizopod species in low densities, and no heterotrophic flagellates, crustaceans or fish,
were observed (Wollmann et al., 2000; Kamjunke et al.,
2004). In the slightly less-acidic lake (117, pH 3.0),
additionally a small pigmented species of Gymnodinium,
the large rotifer Brachionus and the small cladoceran
Chydorus occurred on occasion in considerable densities
(Wollmann et al., 2000). Corixids were excluded from
our analysis as they feed predominantly outside the pelagic
realm. One of the neutral lakes in our study (Lake
Constance) is large, deep, monomictic and meso-oligotrophic and has a food web representative of large open
water bodies. The other neutral lake (Müggelsee) is smaller, shallow and eutrophic (Table I). The neutral lakes,
therefore, represent two typical lake types with
Table I: Morphometric data and pH in the
two acidic and the two neutral lakes
Lake
Area (km2)
Mean depth (m)
pH
111
0.11
4.6
2.6
117
0.96
7
3.0
Constance
Müggelsee
708
476
7.3
101
4.9
7.7–8.5
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pronounced differences in productivity and thus in food
web structure (Carpenter and Kitchell, 1993). Our considerations focus on the epilimnion of the study lakes.
Sampling and data handling
In acidic Lakes 111 and 117, the epilimnion was represented by samples from depths of 0–4 and 0–5 m, respectively. For Lake Constance, average values for the upper
20 m were considered, approximately reflecting the
euphotic zone and epilimnion of the lake. Data from
shallow polymictic Lake Müggelsee were averaged across
depth (mean depth 4.5 m). Seasonal means for the period
April–October were used for all four lakes. The data
describing bacterial biomass, bacterial production and
primary production in Lakes 111 and 117 are from
Kamjunke et al. (2005). The biomass of phytoplankton
and Heliozoa from Lake 111 has been published in
Kamjunke et al. (2004). For Lake 117, biomass data
were taken from Beulker et al. (2003) for phytoplankton,
from Packroff (2000) for ciliates and from Wollmann and
Deneke (2004) for zooplankton. The Lake Constance
and Lake Müggelsee data were obtained from Gaedke
et al. (2002) and Gaedke et al. (2004) for the years 1987–
1993 and 1988–1990, respectively.
The lengths and body masses of organisms from the
acidic lakes are summarized in Table II. The carbon
contents of bacteria, C. acidophila, Ochromonas sp. and
Heliozoa were calculated as described in Kamjunke
et al. (2004). For Gymnodinium sp. and ciliates, the same
factors as for C. acidophila and Heliozoa were used,
respectively. The carbon content of Brachionus was measured (G. Weithoff, personal communication), and the
individual dry weight of Chydorus sphaericus (1450 ng;
Wollmann and Deneke, 2004) was multiplied by 0.5.
Table II: Mean length and body mass of the
dominant organisms in the planktonic food
webs of the acidic lakes (averages ± SD)
Length (mm)
Single-celled bacteria
Filamentous bacteria
0.89 ± 0.19
27.3 ± 7.3
Chlamydomonas
8.4 ± 0.6
Ochromonas
6.2 ± 0.6
Body mass (pg C)
0.02
0.58
23
23
Gymnodinium
12
208
Heliozoa
21.7 ± 2.1
790
Ciliates
20
161
Brachionus
220
160.000
Chydorus
332
725.000
For the neutral lakes, organism size was measured regularly and converted to carbon according to Gaedke et al.
(2002, 2004; literature cited therein). The conversion
factors used were consistent among lakes.
To construct biomass pyramids, we assigned bacteria
to the first trophic level (Gaedke and Straile, 1997). In
the acidic lakes, the mixotrophic flagellate C. acidophila
was regarded to be 80% phototrophic and 20% osmotrophic, and the mixotrophic flagellate Ochromonas sp.
was assumed to be 43% autotrophic, 35% bacterivorous
and 22% herbivorous (ingesting the similar sized C.
acidophila, Tittel et al., 2003). These estimates were
obtained from quantitative carbon flow diagrams [modified after Kamjunke et al. (2004)], which were derived
from field and laboratory measurements at Lake 111
(e.g. Tittel et al., 2003, 2005; Kamjunke et al., 2004,
2005). Because recent results showed that Heliozoa
may grow with bacterial filaments (Bell et al., 2006),
we modified the carbon flow diagram of Kamjunke
et al. (2004) by assuming that 50% of the production of
the bacterial filaments were ingested by Heliozoa. For
Lake Constance, the distribution of consumers across
the different trophic levels was derived from timeresolved, mass-balanced carbon flow diagrams
(Hochstädter, 1997).
Sheldon-type biomass size spectra were constructed
by placing each organism into a log2-scaled size class
according to its individual body mass and summing
the biomass in each size class. Filamentous algae were
allocated to the size class of the individual cells (for
details see Gaedke, 1992). The size spectra of the
various feeding modes were obtained by estimating
the feeding mode of each component species based
on our own measurements (Tittel et al., 2003;
Kamjunke et al., 2004; literature cited therein), an
extended literature review and mass-balanced carbon
flow models (Gaedke et al., 2002). Subsequently, the
biomass of each feeding mode per size class was
summed up. The biomass of mixotrophs and omnivores was split over the respective feeding modes
according to the contribution of each feeding mode.
Sensitivity analyses revealed that the inevitable uncertainties involved in the estimation of the diet compositions of individual species did not affect the overall
pattern inferred from Fig. 5.
Predator–prey weight ratios were calculated for
each feeding interaction using the size range covered
by the predator and prey species, respectively. Each
ratio was weighted by the relative quantitative importance of the feeding interaction for total carbon flux
within the food web. For Lake 111, carbon fluxes
were derived from quantitative carbon flow diagrams
[modified after Kamjunke et al. (2004) to obtain
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seasonal averages and with the additional link
between bacterial filaments and Heliozoa]. For Lake
Constance, the plankton community was subdivided
into 22 trophic guilds ranging from bacteria, through
autotrophic picoplankton, heterotrophic nanoflagellates and phytoplankton (five guilds), ciliates (five
guilds) and rotifers (four guilds), to crustaceans (five
guilds). These trophic guilds were linked by 108 feeding interactions (Lang, 1997). For eukaryotes, the
relative quantitative importance of each trophic link
was roughly estimated from the biomass and sizedependent metabolic activity of the respective predator and prey guilds assuming mostly unselective feeding for omnivorous guilds. The relative importance of
bacteria was inferred from the measured ratio of
bacterial and primary production. These estimates
were cross-checked with more reliable flux estimates
derived from mass-balanced carbon flow diagrams
with a lower taxonomic resolution (Gaedke and
Straile, 1994). No predator–prey weight ratios were
computed for Lakes 117 and Müggelsee because no
suitable data on the quantity of carbon fluxes were
available. We included only lakes into our study for
which food web properties could be quantified based
on fully comparable assumptions, for example in
respect to carbon content, size allocation and growth
efficiencies.
RESULTS
Bacteria and phytoplankton
The biomass of bacteria and phototrophs increased
from low values in Lakes 117 and 111, intermediate
ones in Lake Constance, to high values in eutrophic
Lake Müggelsee (Fig. 1). The ratio of bacterial to phototrophic biomass was approximately 1:3 in Lake
Constance, 1:5 in Lakes 111 and Müggelsee and 1:7
in Lake 117. Taking the sum of bacterial and primary
production as the energy input into the food web, we
observed a trophic gradient with increasing values from
Lake 111 over Lakes 117 and Constance to Lake
Müggelsee. The ratio of bacterial to primary production was 1:5 in Lakes 117 and Constance but 2:1 in
Lake 111. The production-to-biomass ratio (P/B) of
bacteria was high in the acidic lakes and low in Lake
Constance, whereas the P/B of phototrophs was highest
in Lake 117, intermediate in Lake Constance and low
in Lakes 111 and Müggelsee (Fig. 1). Thus, the substantial variability in the relative importance of bacteria
and autotrophs was only partially linked to pH or
trophic state.
Fig. 1. Biomass, production and production to biomass ratios of
bacteria and phototrophs in two extremely acidic mining lakes (111
and 117), one neutral, meso-oligotrophic lake (Constance) and one
neutral, highly eutrophic lake (Müggelsee; n.a. = not analysed).
Functional composition of the entire
planktonic communities
The contribution of bacteria to total planktonic biomass
was lower in acidic (6–9%) than in neutral lakes (12–
15%; Fig. 2). The contribution of phototrophic biomass
to total plankton biomass was 40–44% in the acidic lakes
and Lake Constance, and 57% in eutrophic Lake
Müggelsee resulting in H/A ratios of 1.3–1.5 and 0.75,
respectively. Phototrophic biomass in acidic lakes consisted of the phototrophic fractions of C. acidophila and
Ochromonas sp. (both lakes) and the pigmented, mainly
phototrophic Gymnodinium sp. (Lake 117), whereas filamentous cyanobacteria played a major role in Lake
Müggelsee. For consumers, approximately 45% of plankton biomass was contributed by osmotrophic C. acidophila
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Fig. 2. Composition of total plankton biomass in two extremely acidic mining lakes (111 and 117), one neutral, meso-oligotrophic lake
(Constance) and one neutral, highly eutrophic lake (Müggelsee).
and phagotrophic Ochromonas sp. in the acidic lakes. The
share of heterotrophic protozoa was lowest in Lake 111
(Heliozoa), intermediate in Lake 117 (mainly ciliates) and
Lake Müggelsee and highest in Lake Constance. In contrast to Lake 111, where the biomass of the two rotifers
E. worallii and C. hoodi was too low (<0.1 mg C L–1) to be
included in Fig. 2, a rotifer (Brachionus sericus) and a
crustacean (C. sphaericus) contributed a few percent to
the total biomass in Lake 117. Crustacean plankton
contributed 26–33% to the planktonic biomass of the
neutral lakes, whilst the contribution of rotifers remained
low. Thus, consumer composition was pH-dependent,
whereas H/A ratios depended on the trophic state.
Trophic structure and food chain length
The first trophic level in the acidic lakes consisted of
bacteria, C. acidophila, Gymnodinium sp. (Lake 117) and,
most importantly, phototrophic Ochromonas sp. Bacteria
contributed more to the first trophic level in Lake
Constance than in the acidic lakes (Fig. 3). The second
trophic level was dominated by phagotrophic Ochromonas
sp. under acidic conditions and by ciliates and crustaceans
in Lake Constance. In contrast to the neutral lake, biomass
at the second trophic level was almost as high as that at the
first trophic level in acidic lakes on seasonal average.
Biomass at the third trophic level was extremely small in
Lake 111, relatively small in Lake 117 and large in Lake
Constance which was the only lake with a well-established
fourth trophic level. Accordingly, the average trophic position of the consumers as an indicator of mean food chain
length increased from 2.01 in Lake 111 (pH 2.6) and 2.10
in Lake 117 (pH 3.0) to 2.48 in Lake Constance (pH 8).
Biomass size spectra and predator–prey
weight ratios
The plankton biomass size spectra of the acidic lakes
exhibited distinct peaks and several gaps, i.e. size ranges
where no biomass was detected (Fig. 4). In Lake 111
bacteria, mixotrophic flagellates and Heliozoa were
clearly separated in size. The entire plankton size spectrum ranged over six orders of magnitude, which was
low compared to the Lake Constance and Lake
Müggelsee plankton community (11 orders of magnitude). In Lake 117, Gymnodinium sp. and the ciliates
overlapped in size, and Brachionus and Chydorus extended
the size spectrum to larger body masses compared with
Lake 111. Nevertheless, it remained shorter and more
irregular than in the neutral lakes, given the two gaps
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Fig. 3. Trophic pyramids of biomass of the plankton community of Lakes 111, 117 and Constance (seasonal average). For Lake
Constance, biomass at the fourth trophic level was underestimated because the quantitative carbon flow diagrams did not account
explicitly for piscivorous fish which were at an unnaturally low level due to severe fishing pressure on planktivores (biomass at the fifth
and higher trophic levels not shown).
within the Lake 117 size spectrum and the extremely
high biomass in the size range of the flagellates (Fig. 4).
In contrast to the acidic lakes, plankton biomass spectra
were continuous, i.e. had no size ranges without detectable biomass, and biomass was more evenly distributed
across the size spectrum in Lake Müggelsee and in Lake
Constance, in particular. Phytoplankton ranged from
autotrophic picoplankton to large forms such as the
dinoflagellate Ceratium hirundinella. Protozoa also covered a wide range starting with heterotrophic picoflagellates and ending with large ciliates. Furthermore, the
size spectrum for crustaceans was extended because of
copepod nauplii at the small end and large carnivorous
cladocerans at the other. Overall, plankton biomass
stretched continuously over 34–35 log2 size classes in
the neutral lakes, whereas it was restricted to 16 and 21
partly disjunctive size classes in Lakes 111 and 117,
respectively.
A cross-lake comparison of the size distribution of feeding modes revealed similarities in the small size range and
substantial deviations for medium and large plankters
(Fig. 5). In all lakes, bacteria monopolized the smallest size
classes. They covered an extended size range in the acidic
lakes and in highly eutrophic Lake Müggelsee but were
restricted to a narrow size range in the neutral, oligo-mesotrophic lake where bacterial filaments were less important
and autotrophic picoplankton was abundant. Autotrophs
were extremely restricted in size in the acidic lakes. In
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weight ratios were consistently low, and in some cases
extremely low. Quantitatively important feeding interactions were restricted to values of 20 (1:1; Ochromonas :
Chlamydomonas), 25 (60:1; Heliozoa : flagellates) and
210–211 (1000–2000:1; Ochromonas : single bacteria and
Heliozoa : bacterial filaments, respectively), yielding a
trimodal distribution. In Lake Constance, small predator–
prey weight ratios (<3:1) contributed considerably less (3%)
to total carbon fluxes compared to Lake 111 (21%),
whereas high ratios (>3000:1) contributed 3-fold more
(36%) than in Lake 111 (11%). The frequency distribution
of the predator–prey weight ratios for the Lake Constance
planktonic food web was much broader and more regularly
shaped owing to the higher number of feeding links.
DISCUSSION
Choice of lakes
The lakes compared in this analysis differed in (i) size,
(ii) productivity and (iii) mean acidity.
(i)
Fig. 4. Sheldon-type plankton biomass size distributions of Lakes
111, 117, Müggelsee and Constance.
(ii)
contrast, they spanned five orders of magnitude in the
neural lakes. In the acidic lakes, bacterivores, herbivores
and carnivores partially filled the size range typically covered by autotrophs and did not extend beyond it in Lake
111 (Fig. 5). Therefore, the succession of feeding modes
along the size gradient, considered to be one of the outstanding features of pelagic food webs, was roughly maintained in the acidic lake food webs but feeding modes
strongly overlapped along a shorter size-spectrum.
Considering the size distribution of feeding modes helps
to explain the extreme accumulation of biomass in the
flagellate size range in the acidic lakes (Fig. 4): here, four
feeding modes (osmotrophy, autotrophy, bacterivory and
herbivory) co-occur which is unusual for pelagic food webs.
The frequency distributions of the predator–prey weight
ratios differed greatly between acidic Lake 111 and neutral
Lake Constance (Fig. 6). In Lake 111, predator–prey
713
All lakes are sufficiently large and productive to
potentially sustain four trophic levels. The
volumes of the two acidic lakes were 0.5 106
and 7 106 m3, for which a maximum trophic
position of 3.5–4 is predicted by a cross-lake
comparison (Post et al., 2000). Furthermore, the
differences in diversity are presumably not attributable to differences in lake size, as phytoplankton has a modest exponent in the species–area
relationship (0.13; Smith et al., 2005). This suggests that lake size is not a dominant factor determining the food web properties studied.
Productivity is unlikely to be the major reason for
the absence of a third and fourth trophic level in
the acidic lakes. In the acidic lakes, the seasonal
mean of production at the first trophic level (i.e.
bacterial and primary production) was 20–40
mg C m–3 d–1, which was in the same order as
that measured, for instance, in oligotrophic Lake
Stechlin where four trophic levels were well
expressed (Casper, 1985). Potentially, accumulating biomass at higher trophic levels might be
hampered under extreme conditions by enhanced
metabolic costs for maintenance at each trophic
level. Potentially, building up biomass at higher
trophic levels might be hampered under extreme
conditions by enhanced metabolic costs for maintenance at each trophic level for example, to
maintain the strong gradient of protons and
other ions across the cell membrane. This may
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Herbivores
100
Lake 111
0
100
Lake 117
0
100
Lake
Müggelsee
0
100
Lake
Constance
0
–8
4 fg
–6
–4
–2
0
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2
4
6
8
10
12
1 ng
14
16
18
20
1 µg
22
24 26 28
log2 (body mass) (pg C)
0.25 mg
Fig. 5. Size distributions of the relative importance of feeding modes of the planktonic organisms in two extremely acidic mining lakes
(111 and 117), one neutral, meso-oligotrophic lake (Constance) and one neutral, highly eutrophic lake (Müggelsee).
(iii)
reduce the trophic transfer efficiency from one
trophic level to the next. However, no enhanced
costs were detected for Chlamydomonas acidophila
(Gerloff-Elias et al., 2005), rotifers (Weithoff,
2005) and Heliozoa (Bell et al., in press). Two
well-studied neutral lakes of different productivity
were selected as production is well known to
influence pelagic food web structure (Carpenter
and Kitchell, 1993). These well-established differences in food web structure and function were
used as benchmark to rate the impact of mean
acidity. For most attributes studied, differences in
food web structure were much larger between
acidic and neutral lakes than between neutral
waters, despite their greatly deviating trophic
state and morphology.
Mean acidity remains as the most important difference between lakes, and its major effect was the
strong reduction not only in species numbers but
also in functional groups including crustaceans.
Environmental conditions decreased predatory
diversity, in particular, and removed the higher
trophic levels selectively. The lakes also differed
in respect to mixotrophs, which dominated plankton biomass in the acidic, but not in the neutral
lakes. This is, however, of minor importance for
the present analysis since the contribution of mixotrophs was proportionally allocated to the osmotrophs, autotrophs or phagotrophs, respectively
(for details see Methods).
Bacteria and phytoplankton
A trophic gradient (measured as primary production)
existed across the four lakes, increasing from Lake 111,
through Lakes 117 and Constance, to Lake Müggelsee
(Fig. 1). This trend from low to high similarly existed for
pH, plankton diversity, food chain length and the size
range covered by plankton organisms. Primary production in the acidic lakes, where mixotrophs dominate
frequently (Nixdorf et al., 1998), was at the lower end of
the range observed in many other lakes (Cole et al., 1988).
The ratios of bacterial production to primary production
were within the typical range (20%; Cole et al., 1988),
with the exception of Lake 111 (200%; for discussion
see Kamjunke et al., 2005).
The P/B of bacteria were relatively high in the acidic
lakes and were moderate in Lake Constance. Together
with the low contribution of bacteria to total plankton
biomass, these high ratios indicate a strong top-down
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phototrophs: small cells with high surface to volume
ratios occurred in Lake 117, a wide size range was
found in Lake Constance and large cyanobacterial colonies dominated in Lake Müggelsee (Nixdorf et al., 1992)
within which self-shading further limited production.
Functional composition of the entire
plankton communities
Fig. 6. Predator–prey weight ratios within the planktonic food
webs of Lakes 111 and Constance weighted according to the relative contribution of the individual feeding interactions to overall
carbon fluxes within the respective food webs.
control of bacteria by efficient bacterivores in the acidic
lakes. Biomass of single-celled bacteria was negatively
correlated with Ochromonas biomass in Lake 111
(Kamjunke et al., 2004), and Ochromonas sp. may increase
specific bacterial production (Posch et al., 1999). In contrast, the P/B ratio of phototrophs was extremely low in
Lake 111 (Fig. 1). Growth conditions for phototrophs are
less favourable in this lake because of the very low epilimnetic concentrations of dissolved inorganic carbon
present only as CO2 because of the low pH (Tittel et al.,
2005). Even if phototrophs were intensively grazed, they
would not escape from bottom-up control. Their in situ
growth rates are restricted by CO2, and phosphorus
concentrations and underwater light intensity, all of
which remain low independent of ambient algal density
(Kamjunke et al., 2004; Spijkerman et al. in revision). This
resolves the apparent contradiction with cascade theory
(Oksanen et al., 1981) by having low (phototrophs) and
high (bacteria) P/B ratios at the same trophic level. The
P/B ratio of phototrophs decreased from high values in
well-illuminated Lake 117 to moderate values in Lake
Constance to low ratios in Lake Müggelsee. Among
others, this may be explained by the size of the
The contribution of phototrophs to total plankton biomass and, thus, H/A was similar in the less eutrophic
lakes (111, 117 and Constance) and lower in eutrophic
Lake Müggelsee. This implies a strong influence of lake
trophic state, and a decrease in the H/A ratio with
trophic conditions is well established (e.g. Duarte et al.,
2000). It was attributed to decreasing P/B ratios of
autotrophs (O’Neill and DeAngelis, 1981) and decreasing importance of allochthonous subsidies (Del Giorgio
and Gasol, 1995) with increasing trophy. In Lake 111,
the H/A ratio was high as predicted by the lake’s low
trophic state, although autotrophic P/B ratios were low.
This may be attributed to the high P/B ratios of bacteria
providing an important additional food source for the
dominant primary consumer, to subsidies from benthic
primary production (Kamjunke et al., 2006) and to the
low predation pressure on primary consumers. The latter
was thought to increase H/A ratios in other lakes as well
(Straile, 1998). As predicted, the composition of the consumer community was less influenced by trophic conditions but more sensitive to mean acidity. In neutral lakes,
crustaceans dominated but were almost or entirely
absent in the acidic lakes. Because body size is positively
related to the organizational level, which, in turn, is
negatively related to the ability to survive under extreme
abiotic conditions, the maximum size of organisms
within these lakes declined continuously with decreasing
pH. Thus, large, highly organized organisms, represented by crustaceans (and fish) in this study, are lacking
at low pH, and this has far-reaching consequences for
numerous food web attributes. Lower diversity and an
enhanced risk of extinction of species at higher trophic
levels because of environmental stochasticity and external stressors, which weaken the top-down control, were
also found for other terrestrial and aquatic systems
(Duffy, 2002).
Trophic structure and food chain length
Pelagic systems are well known for comprising four quantitatively important trophic levels (Post et al., 2000) in
contrast to terrestrial systems where biomass is typically
concentrated in three trophic levels (Hairston and
Hairston, 1993). However, in both acidic lakes, consumer
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biomass was concentrated in the second trophic level, and
the third level contributed only 0.3 and 5% to the total
plankton biomass of Lakes 111 and 117, respectively (Lake
Constance: 17% at the third level and >5% at the fourth
level; Fig. 3). This high biomass at the second trophic level
relative to the first is explicable by the relatively high P/B
ratio of the bacteria in Lake 111 and of the bacteria and
phototrophs in Lake 117. In contrast, the second trophic
level was monopolized by Ochromonas sp., which had an
extremely slow turn-over rate (P/B 0.03; Kamjunke
et al., 2004) compared with the first trophic level and
with plankton organisms in general.
Remarkably, the epilimnetic biomass seasonal average
at the first trophic level was similar to the sum of the
biomass at the other trophic levels in all three lakes (111,
117 and Constance) despite the pronounced differences
in food chain length between lakes. In Lake 111, the
biomass of Ochromonas sp. that monopolized the second
trophic level accumulated up to relatively high values.
The extremely low P/B values indicate low loss rates.
This agrees with the lack of efficient metazoan grazers
and the observation that Ochromonas seems to be a poor
food source in laboratory cultures for its potential predators (rotifers and heliozoans; Weithoff, 2004; Bell et al.,
2006). The latter may explain why Ochromonas biomass
accumulates also in Lake 117 even though larger consumers (Brachionus and Chydorus) occur, albeit at low densities. In contrast, in Lake Constance, consumers are
themselves subject to high predatory losses (Gaedke
et al., 2002), which decrease their biomass down to a
level where losses are counterbalanced by sufficiently
high P/B ratios but enable substantial biomass accumulations at the proceeding trophic level. To conclude, the
near absence of a third trophic level under acidic conditions was attributable to the lack of predators capable of
exploiting the production at the second level efficiently,
rather than to a lack of sufficient energy to sustain
another trophic level and/or to the small size of the
water bodies (Post et al., 2000).
Biomass size spectra and predator–prey
weight ratios
Biomass size spectra represent an ataxonomic approach
enabling a comparison of the structure and energetics
of taxonomically strongly deviating pelagic food webs
using the relationship between an organism’s size and its
physiological and ecological properties (Sheldon et al.,
1972; Platt and Denman, 1978; Borgman, 1982;
Gaedke, 1993). The extended size ranges in the size
spectra of the acidic lakes where no organisms were
detected illustrate that major functional types were absent:
autotrophic picoplankton, heterotrophic flagellates, larger
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phytoplankton and crustaceans were lacking in Lake 111,
and ciliates and rotifers were extremely rare. In addition,
even those functional groups present in the food web were
often only represented by one species. Poorly exploited
resources are thought to attract more efficient users, which
in turn favours a more efficient exploitation of available
resources and decreases ‘ecological monopolies’ (Leigh
and Vermeij, 2002) such as the monopolizing position of
Ochromonas. The low plankton diversity observed in the
acidic lakes may be attributable to biotic interactions
such as competition and to abiotic constraints
(Kamjunke et al., 2004), and potentially to the rarity and
isolation of such habitats and their low age (50 years).
However, old natural acidic lakes of volcanic origin exhibit no higher plankton diversity (Pedrozo et al., 2001).
The overall regularity in pelagic food webs of having
osmotrophs in the smallest size classes followed by autotrophs was maintained in the acidic lakes. However, the
second and, where present, third trophic levels in Lake
111 occurred at a point on the planktonic size-spectrum
where phytoplankton dominated in the neutral lakes.
Similarly, the consumers in Lake 117 remained small.
Thus, the flow of matter and energy from small to large
organisms was truncated in the acidic lakes. Remarkably,
the slight increase in pH from Lakes 111 to 117 (pH 2.6
and 3.0) and the reduction in ion concentrations (150 and
23 mg Fe L–1) was immediately reflected in a considerably
greater size range of extant planktonic organisms [Lake
111, 5.7; Lake 117, 8.7 and Lakes Constance and
Müggelsee, 10.5 (with fish 16.8) orders of magnitude,
respectively] but less in the trophic pyramid. The third
trophic level was still weakly represented in Lake 117 since
the biomass of larger organisms was very low.
The predator–prey weight ratios were similar in Lakes
Constance and 111 at the lower end of the size gradient
(bacterivores) but were extremely small at larger prey sizes
in Lake 111. This change with size in predator–prey
weight ratios coincided with that of P/B ratios, which
were normal to high for small organisms (bacteria) and
extremely low for flagellates. It suggests that the presence
of the strong predator–prey interactions, characteristic of
numerous pelagic food webs (Cyr and Pace, 1993),
declined with size in the acidic lakes and confirms the
prediction that food web traits dominated by microorganisms were less affected by the extreme environmental
conditions than those ruled by metazoans.
ACKNOWLEDGEMENTS
We thank Camilla Beulker, Brigitte Nixdorf and the
Special Research Programme ‘Cycling of Matter in Lake
Constance’ (SFB 248) for providing data, and Rita Adrian
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Gaedke, U. and Straile, D. (1997) The trophic position of dead autochthonous organic material and its treatment in trophic analysis.
Environ. Model. Assess., 2, 13–22.
for data and for information on the feeding modes of
planktonic organisms in Lake Müggelsee. Data handling
was supported by Katrin Tirok and Stefan Saumweber.
Special thanks to Guntram Weithoff and Jörg Tittel who
provided valuable background information and stimulating discussions and to Elly Spijkerman, Jörg Tittel and
Elanor Bell for improving the manuscript. This paper is
based on research project no. 0339746 of the Federal
Ministry of Education and Research (BMBF) of Germany.
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Ciso. Limnol. Oceanogr., 36, 860–872.
Geller, W., Klapper, H. and Salomons, W. (1998) Acidic Mining Lakes.
Springer, Berlin.
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