Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient

Abstract

1. Using data from 71, mainly shallow (an average mean depth of 3 m), Danish lakes with contrasting total phosphorus concentrations (summer mean 0.02–1.0 mg P L−l), we describe how species richness, biodiversity and trophic structure change along a total phosphorus (TP) gradient divided into five TP classes (class 1–5: <0.05, 0.05–0.1, 0.1–0.2, 0.2–0.4,> 0.4 mg P L−1). 2. With increasing TP, a significant decline was observed in the species richness of zooplankton and submerged macrophytes, while for fish, phytoplankton and floating-leaved macrophytes, species richness was unimodally related to TP, all peaking at 0.1–0.4 mg P L−1. The Shannon–Wiener and the Hurlbert probability of inter-specific encounter (PIE) diversity indices showed significant unimodal relationships to TP for zooplankton, phytoplankton and fish. Mean depth also contributed positively to the relationship for rotifers, phytoplankton and fish. 3. At low nutrient concentrations, piscivorous fish (particularly perch, Perca fluviatilis) were abundant and the biomass ratio of piscivores to plankti-benthivorous cyprinids was high and the density of cyprinids low. Concurrently, the zooplankton was dominated by large-bodied forms and the biomass ratio of zooplankton to phytoplankton and the calculated grazing pressure on phytoplankton were high. Phytoplankton biomass was low and submerged macrophyte abundance high. 4. With increasing TP, a major shift occurred in trophic structure. Catches of cyprinids in multiple mesh size gill nets increased 10-fold from class 1 to class 5 and the weight ratio of piscivores to planktivores decreased from 0.6 in class 1 to 0.10–0.15 in classes 3–5. In addition, the mean body weight of dominant cyprinids (roach, Rutilus rutilus, and bream, Abramis brama) decreased two–threefold. Simultaneously, small cladocerans gradually became more important, and among copepods, a shift occurred from calanoid to cyclopoids. Mean body weight of cladocerans decreased from 5.1 μg in class 1 to 1.5 μg in class 5, and the biomass ratio of zooplankton to phytoplankton from 0.46 in class 1 to 0.08–0.15 in classes 3–5. Conversely, phytoplankton biomass and chlorophyll a increased 15-fold from class 1 to 5 and submerged macrophytes disappeared from most lakes. 5. The suggestion that fish have a significant structuring role in eutrophic lakes is supported by data from three lakes in which major changes in the abundance of planktivorous fish occurred following fish kill or fish manipulation. In these lakes, studied for 8 years, a reduction in planktivores resulted in a major increase in cladoceran mean size and in the biomass ratio of zooplankton to phytoplankton, while chlorophyll a declined substantially. In comparison, no significant changes were observed in 33 ‘control’ lakes studied during the same period.

Full text

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Freshwater Biology (2000) 45, 201–218
Trophic structure, species richness and biodiversity in
Danish lakes: changes along a phosphorus gradient
ERIK JEPPESEN, JENS PEDER JENSEN, MARTIN SØNDERGAARD, TORBEN LAURIDSEN and
FRANK LANDKILDEHUS
National Environmental Research Institute, Department of Lake and Estuarine Ecology, PO Box 314, DK-8600 Silkeborg,
Denmark
SUMMARY
1. Using data from 71, mainly shallow (an average mean depth of 3 m), Danish lakes
with contrasting total phosphorus concentrations (summer mean 0.02–1.0 mg P L−l),
we describe how species richness, biodiversity and trophic structure change along a
total phosphorus (TP) gradient divided into five TP classes (class 1–5: ?0.05, 0.05–0.1,
0.1–0.2, 0.2–0.4, ?0.4 mg P L−1).
2. With increasing TP, a significant decline was observed in the species richness of
zooplankton and submerged macrophytes, while for fish, phytoplankton and floating-
leaved macrophytes, species richness was unimodally related to TP, all peaking at
0.1–0.4 mg P L−1. The Shannon–Wiener and the Hurlbert probability of inter-specific
encounter (PIE) diversity indices showed significant unimodal relationships to TP for
zooplankton, phytoplankton and fish. Mean depth also contributed positively to the
relationship for rotifers, phytoplankton and fish.
3. At low nutrient concentrations, piscivorous fish (particularly perch, Perca fluviatilis)
were abundant and the biomass ratio of piscivores to plankti-benthivorous cyprinids
was high and the density of cyprinids low. Concurrently, the zooplankton was domi-
nated by large-bodied forms and the biomass ratio of zooplankton to phytoplankton
and the calculated grazing pressure on phytoplankton were high. Phytoplankton
biomass was low and submerged macrophyte abundance high.
4. With increasing TP, a major shift occurred in trophic structure. Catches of cyprinids
in multiple mesh size gill nets increased 10-fold from class 1 to class 5 and the weight
ratio of piscivores to planktivores decreased from 0.6 in class 1 to 0.10–0.15 in classes
3–5. In addition, the mean body weight of dominant cyprinids (roach, Rutilus rutilus,
and bream, Abramis brama) decreased two–threefold. Simultaneously, small cladocerans
gradually became more important, and among copepods, a shift occurred from
calanoid to cyclopoids. Mean body weight of cladocerans decreased from 5.1 ?g in
class 1 to 1.5 ?g in class 5, and the biomass ratio of zooplankton to phytoplankton
from 0.46 in class 1 to 0.08–0.15 in classes 3–5. Conversely, phytoplankton biomass
and chlorophyll a increased 15-fold from class 1 to 5 and submerged macrophytes
disappeared from most lakes.
5. The suggestion that fish have a significant structuring role in eutrophic lakes is
supported by data from three lakes in which major changes in the abundance of
planktivorous fish occurred following fish kill or fish manipulation. In these lakes,
studied for 8 years, a reduction in planktivores resulted in a major increase in clado-
Correspondence: Erik Jeppesen, National Environmental Research Institute, Department of Lake and Estuarine Ecology, PO Box
314, DK-8600 Silkeborg, Denmark.
E-mail: ej@dmu.dk
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E. Jeppesen et al.
202
ceran mean size and in the biomass ratio of zooplankton to phytoplankton, while
chlorophyll a declined substantially. In comparison, no significant changes were ob-
served in 33 ‘control’ lakes studied during the same period.
Keywords: biodiversity, fish, phytoplankton, species richness, zooplankton
Introduction
In recent years, food-web structure and interactions
in the pelagic of lakes have been subject to intense
debate. With a few exceptions (e.g. Hrba ´cek et al.,
1961; Brooks & Dodson, 1965; Brooks, 1969), the pre-
vailing view a decade or two ago was that food webs
are primarily regulated via the available resources
(‘bottom–up’ control). Since then it has become evi-
dent that food webs may be regulated via fish (called
predatory control or ‘top–down’ control) (Carpenter,
Kitchell & Hodgson, 1985; Gulati et al., 1990; Carpen-
ter & Kitchell, 1993). However, opinions vary on the
relative importance of resource and predatory control
along a nutrient gradient. On the basis of the studies
of Fretwell (1977) and Oksanen et al. (1981) of terres-
trial environments, Persson et al. (1988) claimed that
herbivory on phytoplankton depends on the number
of food web links and that the zooplankton grazing
pressure is high in lakes with an even number of
links (e.g. lakes with only zooplankton and phyto-
plankton or lakes with predatory fish, planktivorous
fish, zooplankton and phytoplankton) and low in
lakes with an odd number of links. Predatory control
will, therefore, be strongest in food webs with an
even number of links (two, four, etc.) and resource
control highest in food webs with an odd number of
links. There are several examples supporting the hy-
pothesis (Hansson, 1992; Persson et al., 1992; Wurts-
baugh, 1992), but also many exceptions among both
lakesand streams(Leibold,
Townsend, 1994; McIntosh
Mazumder, 1994; Brett & Goldman, 1996). Among the
reasons for the deviations are behavioural changes of
prey, aiming at reducing the predation risk (McIntosh
& Townsend, 1994), and changes in the composition
of primary producers towards grazing-tolerant/graz-
ing-resistant forms at high grazer density. Moreover,
species at each food-web level may differ in sensitiv-
ity towards potential predators. In addition, some
species cover more than one trophic level or show
ontogenetic shifts in food preference. In nature, food
webs are therefore rarely simple.
1990;
Townsend,
Flecker&
&1994;
Empirical analyses are alternative approaches for
evaluating food-web interactions. Based on statistical
analyses of experimental data, McQueen, Post & Mills
(1986) and McQueen et al. (1989) concluded that re-
source control is highest at the bottom of the food
web and predatory control strongest at the top of the
web. They also suggested that predatory control is
high in oligotrophic lakes and low in eutrophic lakes,
particularly because eutrophic lakes are typically
dominated by cyanobacteria that are difficult for
grazing zooplankton to handle. Elser & Goldman
(1990) and Carney & Elser (1990) then developed the
intermediate control hypothesis, arguing that the
zooplankton grazing pressure on phytoplankton is (a)
low in oligotrophic lakes due to low nutrient
availability and because the zooplankton is domi-
nated by copepods that are less efficient grazers than
large-bodied cladocerans; (b) high in mesotrophic
lakes in which the zooplankton is dominated by the
efficient grazer Daphnia spp.; and (c) low in eutrophic
lakes in which the phytoplankton is dominated by
grazing-resistant species, such as cyanobacteria. In
contrast, Sarnelle (1992) argued that changes in the
biomass of zooplanktivorous fish have their greatest
impact on the phytoplankton (via the zooplankton) in
eutrophic lakes. Likewise, Jeppesen et al. (1997, 1999)
recorded dominance by small-bodied zooplankton
and a low potential grazing pressure on phytoplank-
ton in eutrophic lakes, irrespective of whether the
phytoplankton was dominated by cyanobacteria or
by edible green algae, thus suggesting major top–
down control of zooplankton.
Changes in nutrient loading also result in changes
in community structure at each trophic level or
within different taxonomic groups. To quantify such
changes, numerous indices have been developed (for
a review see Washington, 1984). The most commonly
used are species richness and various indices of di-
versity, and in particular the Shannon–Wiener Index.
Contrasting results have been obtained for the differ-
ent taxonomic units among studies. Some authors
have found a unimodal relationship between species
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A detailed study of Danish lakes along a phosphorus gradient
203
richness and trophic state, peaking at some interme-
diate level in the gradient (Stockner & Benson, 1967),
whereas others record a monotonical decline (Patalas
& Patalas, 1966) or even no significant changes (Eck-
mann & Ro ¨sch, 1998). Diversity indices, and particu-
larly species richness, are sensitive to sample size
(MacArthur & Wilson, 1967), invasion barriers, pH,
latitude, lake area, heterogeneity, predation and dis-
turbance (Hall, Cooper & Werner, 1970; Magnuson,
1976; Fryer, 1985; Rørslett, 1991; Keller & Conlon,
1994) apart from ecological stress factors such as
eutrophication. Variables such as heterogeneity and
pH may, in turn, be influenced by eutrophication,
reflecting a decline in submerged macrophyte cover-
age and enhanced phytoplankton production, respec-
tively. The validity of some of the commonly used
diversity indices has been questioned by several au-
thors (Hurlbert, 1971; Chutter, 1972; Goodman, 1975).
Consequently, Hurlbert (1971) developed an alterna-
tive index, the probability of inter-specific encounter
(PIE) index, incorporating both species richness and
evenness components. The biological relevance of the
PIE index is, therefore, more apparent than that of the
commonly used indices (Washington, 1984), but so
far it has not been used for aquatic ecosystems. In
addition, most studies of species richness and diver-
sity have focused on one or two taxonomic groups,
whereas only a few have compared the response of
several trophic levels/taxonomic groups to changes in
trophic state (e.g. Reed, 1978).
Using survey data from 71, mainly shallow, Danish
lakes, we took an empirical approach to elucidate
how trophic structure, species richness, biodiversity
and the extent of top–down control are affected by
changes in trophic state. We also included case stud-
ies from three lakes in which the biomass of cyprinids
changed markedly as a consequence of fish kill or
manipulation.
Methods
Samples for the analysis of water chemistry and phy-
toplankton and zooplankton communities were taken
fortnightly during summer (1 May–1 Oct). Total
phosphorus and chlorophyll a were analysed on a
depth-integrated sample from the photic zone at a
mid-lake station according to Søndergaard, Kris-
tensen & Jeppesen (1992) and Jespersen & Christof-
fersen (1987), respectively.
Zooplankton densities were determined using
depth-integrated water samples taken with a Patalas
sampler and pooled from one to three stations. De-
pending on the total phosphorus (TP) level, between
4.5 and 9 L of the pooled sample were filtered
through an 80-?m net and fixed in Lugol’s iodine
(1 mL, 100 mL tap water) and 0.5–1 L was settled
overnight in Lugol’s solution. Rotifers and small nau-
plii were counted from the settled samples, whilst all
other zooplankton were counted from net samples.
At least 100 individuals of the dominant zooplankton
species were counted. Length–weight relationships,
according to Dumont, Van De Velde & Dumont
(1975) and Bottrell et al. (1976), were used to estimate
biomass. If possible up to 50 individuals were
measured.
Phytoplankton was counted on Lugol-fixed sedi-
mented water samples (pooled sample from a mid-
lake station in the photic zone) using an inverted
microscope. Biovolume was calculated by fitting the
different species and genera to geometric forms
(Utermo ¨hl, 1958; Edler, 1979; Rott, 1981). A factor of
0.29 was used to convert biovolume (mm3) to biomass
(mg dw) (Reynolds, 1984).
The composition and relative abundance of the
pelagic fish stock in the lakes were determined by
standardized fishing (J.P. Mu ¨ller et al., unpublished)
with multiple mesh (6.25, 8, 19, 12.5, 16.5, 22, 25, 30,
33, 38, 43, 50, 60, 75 mm) gill nets. The length and
depth of each section of mesh was 3 and 1.5 m,
respectively. Fishing was conducted in each lake be-
tween 15 August and 15 September, as previous trial
fishing indicated that the distribution of the fish pop-
ulations was most even during this period (Mu ¨ller et
al., unpublished). Moreover, young-of-the-year fish
were also large enough to be included in the catch by
this time. The nets were set in the late afternoon and
retrieved the following morning. Catch per unit effort
(CPUE) of planktivorous fish was calculated as mean
catch per net.
Species richness of submerged (isoetids, angio-
sperms, mosses and charophytes) and floating-leaved
macrophytes was determined in early August, more
or less corresponding to peak biomass. We divided
each lake into zones (typically 15–22). In each zone,
we conducted observations from a boat using a water
glass or by diving at 10 randomly selected locations
at 25–50 cm depth intervals from the shore to the
macrophyte boundary. At each point, we measured
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E. Jeppesen et al.
204
coverage divided into the following categories: ?1,
1–5, 5–25, 25–50, 50–75, 75–95, ?95% and then
interpolated these data to a coverage for the whole
lake (Jeppesen et al., 1998). For the sake of clarity, the
data were divided amongst five TP categories:
?0.05, 0.05–0.1, 0.1–0.2, 0.2–0.4 and ?0.4 mg P L−1.
The data analysis comprised stepwise regression on
loge-transformed data. In some cases a unimodal rela-
tionship to TP appeared. We then included [loge(TP)]2
as an independent TP variable. To estimate changes
in biodiversity, we used the Shannon–Wiener Index
(H?, bits)
H?n= − ?
s
i=1
ni
nlnni
n,
H?w= − ?
s
i=1
bi
blnbi
b
where niand biare the number and biomass of the ith
species, n and b are the total number and biomass of
all species, and s is the total number of species. We
also used the Hurlbert ‘encounter’ index (PIE, bits)
n−1?1− ?
PIE=
n
s
i=1?ni
n?2?
Results
The lakes studied were, overall, small and shallow
(Table 1). Spearman’s correlation on loge-transformed
data revealed a strong significant positive relation-
ship between TP and total nitrogen (TN), making it
difficult to discriminate between the effect of the two
nutrients on trophic structure. We selected TP as the
independent nutrient variable, as it has been shown
most often to be the best indicator of trophic state in
temperate lakes world-wide (OECD, 1982) as well as
in Danish lakes (Kristensen, Jensen & Jeppesen, 1990).
Total phosphorus was significantly negatively corre-
lated with mean depth, but not related to lake surface
area. As trophic structure and dynamics are substan-
tially affected by lake depth (Keller & Conlon, 1994;
Jeppesen et al., 1997), we included depth as an inde-
pendent variable in our regression analysis to avoid
bias introduced by variations in depth along the TP
gradient. We also included lake area, as species rich-
ness and biodiversity have been shown to be sensi-
tive to the size of the area studied (MacArthur &
Wilson, 1967).
Species richness and diversity
Multiple regressions revealed that fish species rich-
ness was significantly unimodally related to TP (P?
0.0001) and positively
(P?0.0001). Lake area contributed significantly (P?
0.001) if mean depth was excluded, otherwise it did
not (P?0.14). The mean number of fish species in-
creased from six in class 1 to nine in classes 3–4,
followed by a decrease to seven in class 5. The Shan-
non–Wiener Index for fish abundance and biomass
was significantly (P?0.001 and P?0.02, respec-
tively) unimodally related to TP (Fig. 2), and for
abundance only significantly (P?0.01) related to
mean depth. Hurlbert’s index (PIE) was significantly
unimodally related to TP (P?0.003), and positively
related to mean depth (P?0.008) and peaked (0.6
bits) in class 3. In contrast to species richness, lake
area did not contribute significantly to the index
variations in PIE when TP was included as the inde-
pendent variable.
Zooplankton species richness declined consider-
ably (P?0.0001) with increasing TP (Fig. 1), from a
mean of 44 in class 1 to 32 in class 5. The decline was
particularly noticeable for the number of cladoceran
species (14 to eight), although a pronounced decline
was also observed in the species number of copepods
and rotifers (P?0.0001 and P?0.007), respectively.
Multiple regressions revealed that only for rotifers
did mean depth contribute significantly (P?0.0001)
to the variation in species richness, the contribution
of TP then being insignificant (P?0.25). The Shan-
non–Wiener Index, based on both abundance and
related tomeandepth
Table 1 Frequency distribution of some morphometric and chemical data for the 71 study lakes
MaximumMedian Mean 75% PercentileMinimum25% Percentile
Lake area (km2)
Mean depth (m)
TP (mg P L−1)
TN (mg N L−1)
Chlorophyll a (?g L−1)
2.4
3.4
0.21
2.08
87
0.4
2.4
0.15
1.89
52
42
16.5
0.99
5.89
399
0.05
0.9
0.02
0.39
5
1.8
4
0.31
2.83
0.21
1.2
0.08
1.17
30131
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A detailed study of Danish lakes along a phosphorus gradient
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Fig. 1 Box-plot showing the species richness of
phytoplankton, total zooplankton and cladocerans, fish,
submerged macrophytes and floating-leaved macrophytes in
five different TP classes. The full line represents median
values. Also shown are 10, 25, 75 and 90% percentiles of the
variables.
diversity indices for the selected taxa when TP was
included as an independent variable.
Phytoplankton species richness was significantly
(P?0.002) unimodally related to TP, changing from
an average of 84 in class 1 to 95 in class 4, followed by
a decline to 81 in class 5. Mean depth contributed
significantly (P?0.05) in a positive manner to the
variation in species richness when TP was included,
while lake area did not (P?0.3). The Shannon–
Wiener Index, for both abundance and biomass, was
significantly unimodally related to TP (P?0.002 and
P?0.05, respectively). Lake area contributed signifi-
cantly and positively to the variation in the diversity
indices(P?0.0001and
whereas mean depth did not (P?0.5). PIE was, how-
ever, not related to TP (P?0.5).
Marked changes occurred in species richness of
submerged and floating-leaved macrophytes accord-
ing to TP. The number of submerged macrophyte
species declined from an average of 11.7 species in
class 1 to 0.5 in class 5. In addition, the maximum
depth distribution at which submerged macrophytes
were recorded declined significantly (Fig. 3; P?
0.001). Species richness of floating-leaved macro-
phytestended tobe unimodally
significantly) related to TP, ranging from an average
of 2.1 in class 1 over 3.1 in class 3 to 2.5 in class 5.
P?0.02, respectively),
(thoughnot
Trophic structure
The catch of planktivorous fish by weight (CPUEw)
increased significantly (P?0.0001) with TP (Fig. 3).
From the lowest to the highest TP class, CPUEw
increased 10-fold. The increase is mainly attributed to
roach at low and bream at high TP (Fig. 4). The
CPUEwof both bream and roach was significantly
positively related to TP (P?0.001). Mean depth did
not contribute significantly when TP was included as
an independent variable (P?0.2).
With increasing TP, the contribution of piscivorous
fish to total CPUEw decreased substantially (P?
0.0001), from 62% in class 1 to 10–15% in classes 3–5
(Fig. 3). Amongst the piscivores, perch dominated in
the nutrient-poor lakes, whereas northern pike (Esox
lucius L.) and pike perch (Lucioperca lucioperca L.)
were most abundant in nutrient-rich lakes (Fig. 4).
The latter was introduced into Denmark and occurs
in only a few lakes. However, the CPUEwof perch
was negatively related to TP and mean depth, while
biomass, was significantly (P?0.001) unimodally re-
lated to TP (Fig. 2) and positively related to mean
depth (P?0.0001). The indices peaked in class 4
(1.9–2 bits). Likewise, PIE was significantly unimo-
dally related to TP (P?0.0001). It rose with mean
depth (P?0.0001) (Fig. 2) and peaked in class 4 (0.7
bits). Lake area did not contribute significantly (P?
0.2) to the variation in species richness or any of the
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E. Jeppesen et al.
206
CPUEwof pike was unrelated to both variables. Ben-
thivorous ruffe (Gymnocephalus cernuus L.) was sig-
nificantly (P?0.0001) unimodally related to TP,
being highest in class 3. Only for perch did mean
depth contribute significantly to a multiple regression
including TP (P?0.05) as perch biomass increased
with depth.
Besides the changes in biomass, marked changes
occurred in the size/age structure in populations
within the fish community. For example, the average
body weight of perch decreased considerably (P?
0.01) from 56 g in class 1 to 27 g in class 5 (Fig. 5). In
contrast, pike mean weight increased significantly
(P?0.02) with TP, from 650 g in class 1 to 1200–
1500 g in classes 4 and 5. No changes were observed
for pike–perch or ruffe (P?0.8 and P?0.2, respec-
tively). Amongst the cyprinids, the body weight of
both the dominant roach and bream declined signifi-
cantly (P?0.004 and 0.03, respectively) with TP. For
roach this was 132 g in class 1 to 35–56 g in classes 4
and 5, and for bream from 466 g to 188–267 g. No
additional (P?0.15) effect of mean depth on body
weight was found for any species (P?0.15) when TP
was included as an independent variable.
In accordance with the major changes in fish com-
munity structure, the contribution of Daphnia spp. to
the total biomass of cladocerans decreased signifi-
cantly (P?0.0001) with TP (Figs 6 and 7) from 63–
70% in classes 1 and 2 to 38% in class 5. The mean
individual body weight of cladocerans also decreased
accordingly from 5.1 ?g in class 1 to 1.5 ?g in class 5.
The decline in body weight of cladocerans reflected
not only the low relative abundance of Daphnia spp.,
but also a reduction in body weight of the remaining
Daphnia spp. (P?0.01) and of small cladocerans (P?
0.002). The contribution of cyclopoids to the total
abundance and biomass of copepods increased (Fig.
6) from an average of 49% in class 1 to 77% in class 5.
Daphnia spp. and calanoid copepods contributed 70%
of the total biomass in class 1 and 30% in class 5,
while the contribution of rotifers to total biomass was
rather low (10–15%) or constant between classes (Fig.
6). Multiple regressions revealed that CPUE of
plankti-benthivorous fish by numbers contributed
positively and significantly (P?0.0001) to the varia-
tion in the percentage of Daphnia spp., to mean speci-
men biomass of cladocerans and to the biomass
percentage of calanoids to total copepods. TP or TN
Fig. 2 Box-plot showing the Shannon–Wiener diversity index based on abundance (H?n) (upper) and biomass (H?w) (middle) and
the Hurlbert PIE index (lower) for fish, zooplankton and phytoplankton. For further details see the Fig. 1 legend.
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A detailed study of Danish lakes along a phosphorus gradient
207
Fig. 3 August biomass of zooplanktivorous fish (CPUE, catch
in multiple mesh-size gill nets, 14 different mesh sizes
6.25–75 mm in late summer) versus summer mean lake water
concentrations of total phosphorus. Also shown are the
percentage of carnivorous fish, summer mean (1 May–1 Oct)
of zooplankton:phytoplankton biomass ratio, epilimnion
chlorophyll a concentration, Secchi depth and the maximum
depth of submerged macrophytes versus total phosphorus.
Mean?SD of the five total phosphorus groups is shown
(from Jeppesen et al., 1999).
Fig. 4 Box-plot showing mean fresh weight of various fish
species caught in multiple mesh-size gill nets in late summer
(15 August–15 Sept). Note the different scale on the Y-axis.
For further details see the Fig. 1 legend.
0.0001), suggesting lower fish predation pressure in
deep rather than in shallow lakes.
The changes in the zooplankton appear to cascade
to thephytoplankton.
zooplankton:phytoplankton
summer decreased significantly with increasing TP
(P?0.0001) from an average of 0.46 in class 1 to
0.08–0.15 in classes 3–5 (Fig. 3). Mean depth did not
make a significant contribution (P?0.06). With in-
creasing TP, changes occurred in the phytoplankton
community. Dinophytes, chlorophytes, diatoms and
chrysophytesdominated
cyanophytes and diatoms were dominant at interme-
diate TP, with chlorophytes and cyanophytes being
dominant at high TP (Fig. 8).
Consequenty,
biomass
themean
duringratio
atlowTP,whereas
did not add significantly to any of the regressions
(P?0.2). In addition to TP, the average body weight
of cladoceransand the
calanoids amongst copepods and the biomass per-
centage of Daphnia increased with mean depth (P?
percentagebiomass of
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E. Jeppesen et al.
208
Fig. 5 Box-plot showing average body weight of different
fish species (caught in multiple mesh-size gill nets) in five
different TP classes. For further details see the Fig. 1 legend.
In three eutrophic lakes surveyed intensively for 8
years, we observed major changes in fish abundance
during the study period due either to fish kills or fish
manipulation. Data from these lakes may, therefore,
help elucidate the structuring role of fish. In Lake
Engelsholm, cyprinids were removed by netting from
April 1992 to September 1994. In total, 19.2 t fresh
weight, or 438 kg ha−1, were removed, of which
bream constituted 85%. The highest proportion
(11.5 t) was removed in 1992, 2 t in 1993 and 5.7 t in
1994. Cyprinids were calculated at 660 kg ha−1in
1990 and at 138–260 kg ha−1in 1992–96 (Møller,
1998). In Lake Arreskov, a major fish kill occurred in
autumn and winter 1991 (Sandby, 1998). An addi-
tional 4 t of cyprinids were removed in 1995 and
during 1993 and 1995 the lake was stocked with 0+
pike, amounting to a total of 141 individuals per ha.
Cyprinid biomass was calculated at 172 kg ha−1in
1987 and 71 kg ha−1in 1995 (Sandby, 1998). In Lake
Fig. 7 Box-plot showing summer average specimen weight of
various genera and groups of zooplankton in five different
TP classes. For further details see the Fig. 1 legend.
Fig. 6 Time-weighted summer mean biomass and percentage
contribution of zooplankton to total biomass in five different
TP classes.
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A detailed study of Danish lakes along a phosphorus gradient
209
Fig. 8 Time-weighted summer mean biovolume and
percentage contribution of various phytoplankton in five
different TP classes.
reduction in the planktivorous fish biomass resulted
in an increase in mean body weight of cladocerans
and the zooplankton:phytoplankton biomass ratio,
while chlorophyll a decreased (Fig. 9). In comparison,
no significant (P?0.3) changes with time were ob-
served in any of these variables in a reference set of
33 lakes studied during the same period, suggesting
that the changes in the three lakes reflect variations in
fish abundance rather than inter-annual fluctuations
determined by variations in, for example, climate.
Discussion
Species richness and diversity
We observed a different response in species richness
and biodiversity for the various taxonomic groups.
For most of the variables included, species richness
and diversity showed a unimodal relationship with
TP (Figs 1 and 2) and were also variably related to
lake area and/or depth. A different pattern was found
for species richness of zooplankton and submerged
macrophytes, which declined monotonically with TP.
Numerous studies have shown that species rich-
ness of fish in lakes, in accordance with the theory of
island biography and habitat diversity (MacArthur &
Hejrede, 72 kg ha−1of cyprinids were removed dur-
ing 1991–94. In addition, a major, but unquantified,
fish kill occurred under the ice in winter 1995–96
(County of Storstrøm, 1996). In all three lakes, the
Fig. 9 Time-weighted summer mean body weight of cladocerans, zooplankton:phytoplankton ratio and chlorophyll a in three
lakes during 8 years in which major changes have occurred in cyprinid biomass due to fish removal or fish kill, and in 33
other reference lakes (box-plot, see legend of Fig. 1). Arrows show years of major interventions/kills.
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E. Jeppesen et al.
210
Table 2 Correlation analyses of morphometric and nutrient
data based on loge-transformed data
Mean depthTNSurface area
−0.36*
0.49**
–
TP
Surface area
Mean depth
0.64***
ns
ns
ns
–
0.48**
*P?0.05; **P?0.01; ***P?0.001.
This contrasts with the findings of Dodson (1991,
1992) who, by compiling data from 32 European and
66 North American lakes, found that species richness
in both sets of lakes increased with lake size. In
addition, it was unimodally related to phytoplankton
production, which in other studies has been shown to
be linked with TP (OECD, 1982). Furthermore, Dod-
son (1992) found that species richness was higher in
areas rich in lakes. Our study includes only a few
oligotrophic lakes so we cannot exclude the possibil-
ity that a unimodal pattern would emerge if more
nutrient-poor lakes had been included. Another ex-
planation of the high species richness in the lower TP
classes, however, could be that the abundance of
submerged macrophytes increases habitat hetero-
geneity and then, presumably, the species richness. In
shallow mesotrophic lakes in which the area and
volume occupied by submerged macrophytes may be
high, the presence of macrophytes may have a great
impact on overall structural complexity. This con-
trasts with deep lakes in which the macrophytes are
restricted to near-shore areas. In contrast to species
richness, all three selected diversity indices were uni-
modally and positively related to TP. The higher
species richness in the lower TP classes does, there-
fore, not result in higher diversity.
For phytoplankton, both species richness and the
Shannon–Wiener Index were unimodally related to
TP, whereas the importance of lake depth and lake
area varied: diversity increasing with lake area and
species richness with lake depth. As for zooplankton,
different patterns may be found in the literature
(Margalef, 1978). For example, studies of the histori-
cal development in species richness and diversity of
diatoms in Lake Washington also revealed a unimo-
dal relationship with increased eutrophication, while
Margalef (1980) provided evidence of higher diversity
in oligotrophic than in eutrophic lakes and marine
waters. The Shannon–Wiener Index for phytoplank-
ton, based on abundance, varies from 1.0 to 4.5 bits,
but typically falls in the range 2.4–2.6 (Harris, 1986).
Our data are at the lower end of this range, which
may reflect an overall lower diversity in lakes (and
shallow coastal estuaries) compared with the open
ocean (Margalef, 1978, 1980).
Cross-analysis of data from 641 lakes revealed that
lake area contributed most significantly to the varia-
tion in macrophyte species richness in Scandinavian
lakes (Rørslett, 1991). Residual analyses showed low
species richness in lakes with low pH and a unimodal
Wilson, 1967), is strongly linked to lake area (Magnu-
son, 1976; Browne, 1981; Keller & Crisman, 1990;
Bachman et al., 1996). We found fish species diversity
to be independent of lake area, which may, however,
be ascribed to the small variation in lake area charac-
terizing our study lakes (Table 2). How the species
richness and diversity of the fish community change
along a trophic gradient is not clear. While several
studies indicate a decline in species richness with
increasing eutrophication (for a review see Larkin &
Northcote, 1969; Lee, Jones & Jones, 1991), others
have not recorded any changes (Bachman et al., 1996;
Eckmann & Ro ¨sch, 1998). In our study of mainly
shallow lakes, species richness and the three selected
diversity indices were all unimodally related to TP.
Depth added significantly to species richness and
diversity when based on abundance, which might be
explained by a greater number of available niches in
deep lakes.
Most studies have reported an increase in micro-
crustacean zooplankton species richness with lake
size (e.g. Patalas, 1972; Fryer, 1985; Dodson, 1991,
1992). Others have found a closer correlation with
lake depth (Keller & Conlon, 1994), which may be
explained by the larger heterogeneity (Keller & Con-
lon, 1994) and perhaps also the lower fish predation
pressure in deeper lakes (Keller & Conlon, 1994;
Jeppesen et al., 1997). In our study of mainly shallow
lakes, however, lake depth contributed significantly
only to the variation in the species richness of rotifers,
but not of cladocerans or copepods. The higher sensi-
tivity of rotifers to lake depth may reflect the fact that
rotifer species, unlike most microcrustaceans, are
adapted to life in the often oxygen-poor hypolimnion
(Hofmann, 1985), implying that the abundance of
species is probably higher in stratified than in non-
stratified lakes. We found that the species richness of
all selected zooplankton taxa decreased monotoni-
cally with TP and was not independent of lake size.
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A detailed study of Danish lakes along a phosphorus gradient
211
relationship to eutrophication, with mesotrophic–eu-
trophic lakes supporting more species than olig-
otrophic and hypertrophic lakes. In accordance with
the latter, case studies of cultural eutrophication of
mesotrophic lakes have typically shown a loss in
species richness (Ozimek & Kowalczewski, 1984;
Kowalczewski & Ozimek, 1993, Sand-Jensen, 1997).
We also found a significant decrease in macrophyte
species richness in our study. The low contribution of
oligotrophic lakes to our dataset may explain why
we, unlike Rørslett (1991), found a monitonical de-
cline with increasing TP. Hence, a recent study of
Danish lakes including more oligotrophic lakes
showed a tendency towards a unimodal relationship
between species richness and TP (Vestergaard &
Sand-Jensen, unpublished). Compared with the other
taxa in our study, the percentage decline in species
richness with increasing TP was particularly high for
submerged macrophytes. This may reflect the concur-
rent significant decrease in maximum depth distribu-
tion and macrophyte-covered area with eutrophica-
tion and, accordingly, a loss of habitat heterogeneity
for the plants (Fig. 3). For floating-leaved plants,
which are less sensitive to increased turbidity, we
observed a unimodal relationship with TP.
The general unimodal response in species richness
and/or diversity for the different taxonomic groups to
increasing TP or trophic state is to be expected (Dod-
son, 1992): only a few species occur in distilled water
and hypertrophic conditions lead to loss of species
due either to competitive exclusion (Tilman, 1982) or
adverse conditions (e.g. high pH, Hansen, Chris-
tensen & Sortkjær, 1991; and low oxygen in the hy-
polimnion during summer or under ice during
winter, Magnuson, 1976). Various other factors also
play a role, however, and may obscure clear-cut rela-
tionships. We have already mentioned morphometry,
physical structure and biological complexity in gen-
eral. Variation in top-down control also plays a role,
and it is generally believed that high predation or
grazing pressure result in loss of diversity of prey
organisms (Paine, 1969), though the effect seems to
depend on nutrient state (Proulx & Mazumder, 1998).
Increased fish predation may have contributed to the
decline in species richness and diversity of zooplank-
ton at high TP, but it does not explain the decline in
the same variables for phytoplankton as the grazing
pressure on phytoplankton was low at high TP. The
variation in disturbance of various kinds may also be
important and it is generally accepted that species
richness and diversity are highest at intermediate
disturbances (Connell, 1978).
Trophic structure
The increase in CPUEwand the decline in the percent-
age of piscivores with increasing TP agree with the
results from other studies in both temperate and
subtropical regions (Bays & Crisman, 1983; Hanson &
Peters, 1984; Persson et al., 1988; Quiros, 1990; Bach-
man et al., 1996). The change in the fish community
from dominance by perch and pike in mesotrophic
lakes to exclusive dominance by cyprinids in eu-
trophic lakes is well-documented in other studies of
North European lakes (Sva ¨rdson, 1976; Leach et al.,
1977; Persson, 1983; Persson et al., 1988). The superi-
ority of roach in eutrophic lakes is attributed to a
high potential growth rate along with a higher preda-
tion efficiency on cladocerans (Persson, 1983) and an
ability to exploit smaller zooplankton prey (Stenson,
1979; Lessmark, 1983). Moreover, cyprinids are omni-
vorous, while large perch are piscivores. Finally, the
loss of habitat complexity with the disappearance of
submerged macrophytes, and thus increased turbid-
ity, disfavours percids and, furthermore, augments
intra-specific competition among them (Persson et al.,
1988).
The enhanced dominance of cyprinids was accom-
panied by a decline in average size of both cyprinids
and perch. The decline probably reflects enhanced
competition for food, which in turn may be mediated
by reduced predation of piscivores on young fish.
Thus, the fraction of large piscivorous individuals
among the perch population declined. In addition,
the average weight of pike increased considerably,
probably as a result of enhanced cannibalism due to
reduced structural complexity (less macrophytes)
and, consequently, the loss of refuges (Grimm &
Backx, 1990). As large pike control small prey fish less
efficiently than small pike (Grimm & Backx, 1990), the
incapability to control young planktivores decreased.
It is generally believed that ruffe biomass increases
with increasing TP (Biro, 1977; Hartman & Nu ¨mann,
1977; Persson, 1983; Bergman, 1991). Our study cov-
ered a larger TP gradient than in previous work,
however, and showed a significant unimodal rela-
tionship peaking in class 3 (0.1–0.2 mg P L−1). The
ruffe is benthivorous (Johnsen, 1965; Bergman, 1991)
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E. Jeppesen et al.
212
and a competitor to young benthivorous perch. It has
been argued that an increase in ruffe abundance with
increasing TP reflects the fact that the foraging ability
of ruffe (unlike that of perch) is largely independent
of light (Bergman, 1991). Thus, ruffe may forage effec-
tively in turbid eutrophic lakes (Bergman, 1991;
Bergman & Greenberg, 1994). However, in eutrophic
lakes ruffe faces other competitors. The observed de-
cline at high TP is probably caused by the increase in
the abundance of bream (Fig. 3). The bream is sup-
posedly a superior competitor in these lakes, both
because it is an efficient predator on benthic inverte-
brates and because it, unlike ruffe, feeds efficiently in
the pelagic and therefore may alternate between the
benthic and pelagic feeding mode. That ruffe is an
inferior competitor at high cyprinid density is evident
from several biomanipulation experiments showing
high abundance of ruffe during the first 1–2 years
after cyprinid removal, followed by a major decline
when young perch, after having initially taken advan-
tage of the ‘empty niche’ in the pelagic, reached the
benthivorous state (E. Jeppesen and M. Søndergaard,
unpublished). The enhanced importance of pike–
perch in eutrophic lakes is well-known from other
European lakes (Sva ¨rdson, 1976) and in accordance
with their adaptations (high light sensitivity of their
eyes, Ali, Ryder & Anctil, 1977) for foraging effi-
ciently in turbid water.
Confirming most other
biomass increased with increasing TP (McCauley &
Kalff, 1981; Hanson & Peters, 1984). In contrast to a
number of studies (Brooks, 1969; Bays & Crisman,
1983), however, we did not find any differences in the
proportion of major taxa to biomass. Rotifers typi-
cally constituted 10–15% of biomass in all TP classes,
thisbeing consistentwith
mesotrophic Norwegian lakes (Hessen, Faafeng &
Andersen, 1995). The results from the Danish and
Norwegian lakes suggest that changes in the contri-
bution of rotifers are generally not to be expected
over a substantial TP gradient (3–1000 ?g P L−1) in
north temperate lakes, which contradicts studies from
subtropical lakes, in which an increase in rot-
ifer:zooplankton biomass was found with increasing
trophic state (Bays & Crisman, 1983). Some studies
have found an increasing share of cladocerans with
TP at the expense of copepods (Patalas, 1972;
Rognerud & Kjellberg, 1984; Straile & Geller, 1998). In
our study, the contribution of cladocerans and cope-
studies,zooplankton
resultsfrom oligo-
pods to total biomass in the five TP classes ranged
from 50 to 58% and 34 to 42%, respectively, and the
contribution of cladocerans tended to decrease and
copepods to increase slightly, though not signifi-
cantly, with increasing TP. Major changes occurred in
the contribution of calanoids and cyclopoids to cope-
pod biomass, however, as well as in the contribution
and mean individual weight of large cladocerans. A
shift from calanoids to cyclopoids with increasing
trophic state has been suggested by several authors
(Gliwicz, 1969; Patalas, 1972; Bays & Crisman, 1983)
and has been related to changes in food size spectra
(Pace, 1986) or predation (Hessen et al., 1995;
Jeppesen et al., 1997). Owing to their ability to make
evasive jumps, cyclopoids are often less vulnerable to
fish predation than calanoids (Winfield et al., 1983),
although there are exceptions (Brooks, 1969). More-
over, juvenile cyclopoids might be superior to
calanoids at high food concentrations (Santer & Van
den Bosch, 1994), and increased predation on juvenile
calanoids by adult cyclopoids may further reduce
calanoid abundance (Straile & Geller, 1998). Several
authors record an increased share of small cladocer-
ans with increasing trophic state (e.g. McNaught,
1975; Patalas, 1972). This is often attributed to en-
hanced fish predation (Brooks, 1969; Lyche, 1990).
Accordingly, we found an increase in the contribu-
tion of Daphnia spp. among cladocerans and of clado-
ceran mean body weight after being released from
fish predation after fish removal and fish kills (Fig. 9).
World-wide, biomanipulation experiments in eu-
trophic lakes have shown similar results provided
that fish biomass was substantially reduced (e.g.
Benndorf, 1990; Hansson et al., 1998).
The changes in the
structure and biomass appeared to cascade down
to phytoplankton. Assuming that during summer
cladocerans ingest organic carbon corresponding to
100% of their biomass per day (compared with cope-
pods 50% per day and rotifers 200% per day) (Hansen
et al., 1992) and assuming that they exclusively feed
on phytoplankton, then grazing amounted to 59% of
phytoplankton biomass per day in class 1 and 16–
19% per day in classes 4 and 5. The latter is so low
that zooplankton probably have little effect on phyto-
plankton growth, while in class 1 and 2 lakes it seems
probable that zooplankton apply a considerable graz-
ing pressure to phytoplankton. In addition, the ob-
served reduction in the individual weight of clado-
zooplanktoncommunity
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A detailed study of Danish lakes along a phosphorus gradient
213
cerans and Daphnia spp. presumably further ad-
versely affected the grazing capacity of phytoplank-
ton,because small-bodied
efficient grazers on large-sized phytoplankton than
the large-bodied forms (Gliwicz, 1977, 1990). How the
alteration in fish community structure and biomass,
mediated by the changes in trophic state, affects her-
bivory on phytoplankton has been the subject of
extensive discussion (DeMelo, France & McQueen,
1992; Carpenter & Kitchell, 1992). Our data, as well as
those of Leibold (1990) and Sarnelle (1992), suggest a
more significant effect in eutrophic lakes than in
mesotrophic lakes.
Several authors have argued that filamentous
cyanobacteria prevent grazer control by zooplankton
in eutrophic lakes, which may explain a decrease in
herbivory from mesotrophic to eutrophic lakes (Elser
& Goldman, 1990; Carney & Elser, 1990). Supporting
this view, controlled laboratory experiments have
shown that dense cyanobacterial assemblages can pre-
vent the growth of large cladocerans (e.g. Lampert,
1981; Dawidovicz, Gliwicz & Gulati, 1988; Gliwicz,
1990). Furthermore, in field experiments Daphnia spp.
have occasionally failed to respond to minor, and in a
few cases even to major, reductions in planktivorous
fish populations (e.g. Van Donk et al., 1990; Riemann
et al., 1990; Moss, Stansfield & Irvine, 1991; DeMelo,
France & McQueen, 1992). The results from Danish
lakes indicate, however, that the role of cyanobacteria
in the decline in herbivory from mesotrophic to eu-
trophic lakes is considerably less significant than that
of fish. First, the zooplankton:phytoplankton ratio and
the size of cladocerans are low not only in eutrophic
lakes dominated by cyanobacteria but also in the most
nutrient-rich lakes dominated by edible green algae.
Second, a reduction in fish predation on zooplankton,
due either to the removal of cyprinids or to fish kills,
caused a major increase in the abundance and average
size of cladocerans and a decrease in phytoplankton
biomass in eutrophic lakes, irrespective of whether
cyanobacteria or chlorophytes dominated previously
(Jeppesen et al., 1997; Søndergaard, Jeppesen &
Jensen, 1998; Jeppesen et al., 1999; authors’ unpub-
lished data). Finally, whereas in Danish lakes CPUEw
contributed highly significantly to the variation in the
zooplankton:phytoplankton
mean size, the percentage contribution of cyanobacte-
ria to the total biomass of phytoplankton did not
(Jeppesen et al., 1997).
cladoceransareless
ratio andcladoceran
The strong evidence of a decrease in herbivory,
mediated by planktivorous fish from mesotrophic to
hypertrophic lakes implies that the cascading effect of
fish manipulation on phytoplankton in shallow lakes
will be greatest under hypertrophic conditions,
though the benefit of such a manipulation may be
transient as planktivorous fish are highly successful in
such lakes (Fig. 3; Kitchell et al., 1977; Leach et al.,
1977; Persson et al., 1988; Jeppesen et al., 1990). There-
fore, a return to a turbid state and to low zooplankton
grazing seems likely, even though it may be some-
what delayed in shallow lakes with an extensive
growth of submerged macrophytes (Meijer et al.,
1994). The data in Fig. 3 suggest that the likelihood of
obtaining high zooplankton grazing in shallow lakes
increases markedly when summer mean TP drops
below about 0.1 mg P L−1. Therefore, the prospects of
long-term success of biomanipulation in shallow lakes
are most probably greatest below this threshold
(Jeppesen et al., 1990). The results shown in Figs 3–8
may leave the impression that the shift from clear to
turbid conditions occurred gradually with increasing
TP. However, several case studies of shallow lakes
have shown a step-wise shift and, within certain
nutrientregimes (typically
Jeppesen et al., 1990), lakes may shift between the two
states (Moss, 1990; Jeppesen et al., 1990; Scheffer,
1990), this being the case in Danish lakes (Jeppesen et
al., 1990).Lake-specific
thresholds, and the fact that we also included some-
what deep lakes, may explain the lack of step-wise
shifts in the present study.
In summary, species richness and diversity of most
of the selected taxonomic groupings were unimodally
related to TP in the nutrient range from 0.02 to 1.0 mg
P L−1and, moreover, often related positively to mean
depth and/or lake area. Only the species richness of
zooplankton and submerged macrophytes deviated
by showing a monotonical decline with increasing TP.
Major changes occurred in the community structure
and size distribution of fish, which apparently
cascaded to the lower trophic levels. The share of
piscivores declined markedly and, moreover, the
size of the predatory fish changed towards those
size classes less likely to control cyprinids (larger
pike and smaller perch). Enhanced predation ap-
peared to lead to a marked reduction of the zooplank-
ton:phytoplankton biomass ratio and the grazing
0.5–0.15 mgP L−1;
differencesin nutrient
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E. Jeppesen et al.
214
pressure upon phytoplankton. The latter may have
been exacerbated by a decline in the size of grazing
zooplankton.
Acknowledgments
The authors thank the counties for access to data
from the Survey Programme of Danish Lakes and
Martin R. Perrow for valuable comments. The study
was supported by the Danish Natural Science Re-
search Council (Grant 9601711) and the research pro-
gramme ‘The Role of Fish in Ecosystems, 1999–2001’,
funded by the Ministry of Agriculture, Fisheries and
Food. They thank Anne Mette Poulsen, Kathe
Møgelvang and Henrik F. Rasmussen for skillful
technical assistance.
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