Macrophyte decline in Danish lakes and streams over

the past 100 years

KAJ SAND-JENSEN*, TENNA RIIS*{{ , OLE VESTERGAARD* and

SéREN ERIK LARSEN{*Freshwater Biological Laboratory, University of Copenhagen, Helsingùrsgade 51, DK-3400 Hillerùd, Denmark;

and {National Environmental Research Institute, Vejlsùvej 25, DK-8600, Silkeborg, Denmark

Summary

1 Freshwater habitats in cultivated and densely populated lowland regions of

Europe have experienced profound changes during the last 100 years. We take

advantage of the long interest in aquatic plants in Denmark to compare the sub-

merged ¯ora in lakes and streams in 1896 and 1996.

2 Most of the lakes which contained a diverse submerged vegetation 100 years ago

now have the high phytoplankton biomasses and summer transparencies below 2.0

m characteristic of eutrophication. The majority of 17 lakes included in both old

and recent studies have lost all or most of their submerged species. Species richness

for those lakes that were vegetated did not, however, di�er signi®cantly between

old and recent studies.

3 Species richness declined markedly in the 13 streams included in both studies.

Over all sites, there was also a signi®cant decline of species richness per locality.

Potamogeton species declined from 16 to 9, despite an 8-fold increase in the number

of sites surveyed.

4 Similar compositions and rank-abundances of Potamogeton species in lakes and

streams studied 100 years ago re¯ect suitable growth conditions and mutual

exchange of propagules. Today, low habitat diversity and frequent disturbance in

streams and low recruitment from lakes favours only robust, fast-growing species

capable of regrowth following weed cutting and dredging.

5 A positive interspeci®c relationship observed in the contemporary stream vegeta-

tion between mean local abundance and number of occupied sites was probably

promoted by redistribution of plants as a result of disturbance and e�cient disper-

sal in the interconnected stream network.

6 The freshwater macrophyte ¯ora in north-west Europe presently includes a high

proportion of rare species which are threatened by extinction. Both species typical

for oligotrophic conditions (e.g. P. ®liformis and P. polygonifolius) and another

group of large, slow-growing species (e.g. P. alpinus, P. lucens, P. praelongus and P.

zosterifolius), were once common but are now infrequent, while other transient spe-

cies have remained rare (e.g. P. acutifolius, P. colouratus, P. densus and P. rutilus).

The presence of many species that barely survive in small and distant populations

will make re-assembly of submerged aquatic communities di�cult.

Key-words: disturbance, eutrophication, freshwater macrophytes, historical changes

Journal of Ecology (2000) 88, 1030±1040

Correspondence: K. Sand-Jensen, Freshwater Biological Laboratory, University of Copenhagen, Helsingùrsgade 51, DK-

3400 Hillerùd, Denmark (fax� 45 48241474) or T. Riis (e-mail t.riis@niwa.cri.nz).{Present address: National Institute of

Water and Atmospheric Research Ltd (NIWA), PO Box 8602, Christchurch, New Zealand.

Journal of

Ecology 2000,

88, 1030±1040

# 2000 British

Ecological Society

Introduction

At the end of the 1800s there was rich and wide-

spread submerged vegetation in the small lakes and

streams of lowland Denmark (Baagùe & Ravn

1895±96) and a diverse aquatic ¯ora in other Danish

and English localities (Nielsen 1872±74; Raunkiñr

1895±99; Andersen 1910; Ostenfeld 1913;

Mountford 1994; work cited in Preston 1995).

Palaeolimnological studies of plant macrofossils in

sediments from 10 Danish lakes con®rm the pre-

sence of a well-developed submerged ¯ora 100±200

years ago, which is now absent following heavy

eutrophication (Klein 1993; Anderson & Odgaard

1994; Odgaard et al. 1997).

Stream sediments, however, are mobile and can-

not provide a cumulative, chronological series of

plant remains such as is possible in lakes (Anderson

1993). There are, however, many historical publica-

tions, excursion reports and herbarium collections

that record the past occurrence of submerged species

in Denmark. Moreover, recent extensive surveys of

Danish lakes (Vestergaard 1998) and streams (Riis,

Sand-Jensen & Vestergaard 2000) enable testing of

how species richness and relative abundance of sub-

merged plants have changed.

The past 100 years have brought profound envir-

onmental changes to freshwater environments (e.g.

Wetzel 1983; Sand-Jensen & Pedersen 1997; Moss

1998). As in other parts of Europe and North

America industrial production and population den-

sity have increased so that most waste products are

now removed through freshwaters (Sand-Jensen &

Lindegaard 1996; Kamp-Nielsen 1997) albeit with

reduced input of organic pollutants recently

(Kristensen & Hansen 1994). There is extensive

application of fertilizers and drainage of wet mea-

dows has also increased enormously (Madsen 1995)

as has management of streams (98% cited by

Brookes 1984), for instance by regular weed cutting

and dredging.

Such changes have presumably led to the substan-

tial changes observed in species composition, species

richness and cover of the aquatic vegetation (Olsen

1964; Chambers & Kal� 1985; Rùrslett 1991;

Barrat-Segretain 1996). The number of suitable

habitats has diminished over the past 100 years, but

if habitat destruction has taken place randomly, the

rank species abundance may not have changed with

the rarest species (transients) disappearing by chance

(Grime 1998). Relative abundance may, however,

have changed as the progressive environmental

changes have a�ected individual species di�erently

(Roelofs 1983; Bobbink et al. 1998). In eutrophic

lakes, for example, small and slow-growing species

have often disappeared, while robust, fast-growing

species, capable of forming a canopy just below the

water surface, have survived (Adams & McCracken

1974; Phillips et al. 1978; Sand-Jensen 1997). A few

fast-growing species with a high capacity for disper-

sal and colonization may also be favoured by the

disturbed conditions in managed streams (Henry &

Amoros 1996; Henry et al. 1996; Barrat-Segretain et

al. 1998). The many plant species which are now

restricted to a few localities may be prone to extinc-

tion and may well be unable to expand into newly

favourable sites (Thompson & Hodgson 1996;

Gaston & Curnutt 1998).

The availability of historical data from Danish

lakes and streams allows us to evaluate changes in

the patterns of submerged vascular plants over the

past century. Special emphasis is placed on the spe-

cies-rich genus Potamogeton, for which comprehen-

sive and accurate information is available from past

studies. Although strong environmental changes

have taken place world-wide, such broad-scale

changes of the richness of the aquatic ¯ora have not

been studied before. We also test whether directional

changes of abundance and relative rank of

Potamogeton species are as expected from their life

history strategies, the overall nutrient enrichment of

freshwaters, and the intense disturbance of streams.

The relationship between local abundance and geo-

graphical range size in the contemporary stream

¯ora was also evaluated to complement our other

analyses of stream vegetation (detailed in Riis et al.

2000; Riis & Sand-Jensen. 2000).

Materials and methods

Information on the presence of submerged vascular

plants in lakes and streams distributed throughout

Denmark was compiled from literature published

between 1870 and 1929. We refer to this as data

from 1896 (corresponding to the most comprehen-

sive study, Baagùe & Ravn 1895±96) although data

from ®eld studies between 1870 and 1927 are

included. Most of these were published in Danish in

Botanisk Tidsskrift (Journal de Botanique,

Copenhague), either as normal articles or as reports

from excursions organized by the Danish Botanical

Society. We examined all specimens and written

records from the period kept in the main herbarium

in the Botanical Museum, Copenhagen, and used

this information to check and augment the pub-

lished data. We omitted studies in which the aquatic

vegetation of lakes had only been studied close to

the shore or in surface waters and data from ponds

(<1ha) and acid (pH<5.5), saline (>3 g NaCl

Lÿ1) or arti®cial lakes, whose vegetation is unrepre-

sentative of the majority of natural freshwater lakes.

Danish streams are usually small and shallow,

allowing comprehensive description of their vegeta-

tion.

Species identi®cation in the old studies is likely to

be accurate, because the excellent Danish ¯ora avail-

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Journal of Ecology,

88, 1030±1040

able (Raunkiñr 1890) had keys for identi®cation of

most aquatic plants and its species delimitation clo-

sely resembles that used today (Moeslund et al.

1990). Potamogeton species were the subject of

much interest and information on the group is likely

to be particularly accurate and comprehensive

(Baagùe & Ravn 1895±96; Raunkiñr 1895±99).

Species of Callitriche were excluded because ¯owers

or seeds are required for identi®cation, and plants

collected in the ®eld are usually sterile. We compiled

historical data from 40 lakes and 27 streams.

Data from studies of 66 lakes between 1983 and

1993 were compiled by Vestergaard (1998) and

include careful recordings of aquatic plants along

several depth transects. Studies at 208 stream local-

ities from 1996 and 1997 include careful recording

of the presence of aquatic plants in 150±250 quad-

rats (20� 20 cm) along 10±20 transects across 100

m-long stretches at each stream locality (Riis et al.

2000). These recent studies are collectively referred

to as 1996 data (100 years after the historical data

with which they are compared).

The current mean local abundance and the geo-

graphical range size of each species was calculated

based on the abundance and presence at the 208

stream localities. The local abundance of a species

was calculated as the proportion of the 150±250

quadrats at a particular locality, and the mean local

abundance as the average abundance at those local-

ities where it occurs. The geographical range of a

species was calculated as the proportion of the 208

localities at which it was found.

For the larger lakes the contemporary surveys are

more thorough than in the past, with two persons

spending between 1 and 3 days (c. 8±24 h), including

Scuba diving, at each site. In recent surveys two

people spent about 5 h at each stream. Two pairs of

botanists conducted the classical study of 42 fresh-

water localities during a 14-day excursion in 1895

(Baagùe & Ravn 1895±96). Allowing for longer

working days but slower transport, we estimate they

spent a total of 224 h at the sites, suggesting a simi-

lar mean e�ort per locality (and thus equal likeli-

hood of ®nding a species if it was present) to the

contemporary surveys.

We used a randomization procedure to facilitate

comparison between old and recent studies and

between lake and stream studies, irrespective of dif-

ferences in number of localities. Mean number and

2.5±97.5% percentiles in the relative abundance of

Potamogeton species were calculated to form a 95%

con®dence interval for the contemporary frequency

had the same number of sites been used, by ran-

domly drawing 27 lake or 40 stream localities 1000

times from the greater number surveyed. Similar

procedures were used to compare lake and stream

data within each survey period.

The ability of the past and present vegetation to

withstand physical disturbance was compared based

on the ability of Potamogeton species to recolonize

an open stream. Two numerical indices (scores: 1±

3), describing the capability of each species to dis-

perse between sites (by shoot fragments, specialized

short shoots and seeds) or locally (via the root-rhi-

zome system) were derived from Riis & Sand-Jensen

2000, their table 4). Evaluation of the response to

eutrophication was based on their predicted perfor-

mance in the turbid waters expected when phyto-

plankton growth is enhanced. Two morphological

indices (scores: 1±3) of height and growth form of

the species (Riis & Sand-Jensen 2000, their table 4),

describe the ability to grow up through the water

column and spread their canopy close to or on the

water surface.

We acknowledge that these morphological indices,

although based on all the available literature, pro-

vide only a crude description of ecological strategies

and the performance of Potamogeton species under

disturbed and turbid conditions, as they do not

account for di�erences in growth capacity or the

ability to tolerate weed cutting, ¯ow peaks, dred-

ging, reducing/anoxic sediments and overgrowth of

epiphytic communities.

Results

DECLINE OF SPECIES RICHNESS IN THE

SAME LOCALITIES

Species richness of all submerged vascular plants,

and of Potamogeton species in particular, has

declined signi®cantly in nearly all of the 17 lakes

that were surveyed on both occasions (Fig. 1). All of

these had submerged vegetation in 1896, but seven

have since lost all submerged vegetation and a

further three now contain only 1±3 species.

The prevalence of lakes with high phytoplankton

biomass and unclear water is demonstrated by med-

ian summer chlorophyll concentration of 55mg mÿ3

and a median summer Secchi-transparency of 0.85m

for 182 Danish lakes sampled in 1999 (J. P. Jensen

1999, personal communication). Only 13% of these

lakes had transparencies exceeding the 2.0m

required for development of a diverse submerged

vegetation (Vestergaard 1998). The 66 lakes included

in our contemporary study, however, had clearer

than average water with 33% having a Secchi-trans-

parency greater than 2.0m (and 75%>0.85m;

Vestergaard 1998).

Mean species richness of submerged vascular

plants has also declined signi®cantly in streams (13.6

vs. 7.0, Fig. 1). The mean number of Potamogeton

species declined even more markedly (6.7 vs. 2.6,

Fig. 1) with the mean ratio of Potamogeton species

to all submerged species falling from 0.59 (�0.09,

SE) to 0.38 (�0.08).

1032Macrophyte

decline in Danish

lakes

# 2000 British

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Journal of Ecology,

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SPECIES RICHNESS AT ALL VEGETATED

LOCALITIES

Figure 2 shows frequency distribution for species

number in sites at which submerged plants were pre-

sent. In lakes, neither total species number nor that

of Potamogeton species alone, was signi®cantly dif-

ferent between surveys (Mann±Whitney, P>0.05;

Fig. 2). Species richness in streams was much higher

100 years ago than it is today (Mann±Whitney, P<

0.0001; Fig. 2).

RELATIVE OCCURRENCE OF POTAMOGETON

SPECIES

The relative occurrence of each Potamogeton spe-

cies, calculated as the proportion of vegetated lakes

Fig. 1 Number of submerged species and Potamogeton species alone in the lakes and streams that were studied in both 1896

and 1996. The diagonal line marks the 1±1 relationship between past and present species number. Species number has

declined signi®cantly over the 100 years in all four instances (signed rank test, P<0.05).

Fig. 2 Frequency distribution of number of submerged species and of Potamogeton spp. in a large number of vegetated

lakes and streams studied in either or both 1896 (*) and 1996 (W).

1033K. Sand-Jensen

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Journal of Ecology,

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and streams in which it occurred is given in Table 1

together with 95% con®dence intervals for reduced

data sets derived from randomization procedures

(see methods).

Comparing only species present in at least one of

the appropriate data sets, 10 Potamogeton species

had a signi®cantly higher occurrence in 1896 in

streams than in lakes, while the remaining six spe-

cies did not di�er signi®cantly (Table 1).

Potamogeton species observed in streams declined

from 16 to nine despite an eight-fold increase in sur-

vey sites. All but one declined signi®cantly over

time. Three Potamogeton species in lakes occur sig-

ni®cantly more frequently now than in the past and

only seven of the 14 species declined signi®cantly,

leading to a reversal of the 1896 situation.

Consequently all except one species now occur

markedly less often in streams than in lakes (Table

1).

Among the individual species, Potamogeton zos-

terifolius was very common in lakes and streams stu-

died 100 years ago, while it is rare today (Table 1),

and P. alpinus, P. ®liformis, P. frisii, P. natans, P.

lucens and P. polygonifolius have also declined signif-

icantly in both habitats (P<0.05). Species typical

for eutrophic sites such as Potamogeton crispus, P.

natans, P. pectinatus and P. perfoliatus, however,

remain relatively abundant.

RANK-ABUNDANCE AND DIRECTIONAL

CHANGES AMONG POTAMOGETON SPECIES

We found signi®cant correlations between the rela-

tive abundance of individual Potamogeton species in

lakes and streams in old and recent studies (Table

2). Correlations in species abundance were stronger

between lakes and streams studied 100 years ago

than recently, mainly due to profound decline of the

stream vegetation.

Highly signi®cant linear relationships were

observed between log relative abundance and falling

rank of Potamogeton species in lakes and streams in

the two study periods (Fig. 3). The negative slope of

Table 1 Mean frequency of occurrence of Potamogeton species in streams and lakes in 1896 and 1996. For comparison

between di�erent studies, a randomization procedure (see text) was used to calculate 2.5% and 97.5% con®dence limits of

occurrence. n � number of original localities, N � number of localities sampled in the randomization procedure. Roman

numbers indicate columns used in comparisons: I, lakes vs. streams in 1896 (using 27 lakes selected at random from 40

sampled); II, lakes 1896 vs. 1996; III, streams 1896 vs. 1996; IV, lakes vs. streams 1996

Original mean frequency C.L. of occurrence in randomization procedure

Species

I

Stream

1896

n� 27

II

Lake

1896

n� 40

III

Stream

1996

n� 208

IV

Lake

1996

n� 66

I

Lake

1896

N� 27

II

Lake

1996

N� 40

III

Stream

1996

N� 27

IV

Stream

1996

N� 66

P. acutifolius 0.11 0.00 0.00 0.03 ± 0.00±0.05 ± ±

P. alpinus 0.41 0.15 0.00 0.08 0.07±0.22 0.03±0.13 ± ±

P. crispus 0.41 0.45 0.30 0.47 0.33±0.55 0.38±0.55 0.15±0.48 0.21±0.39

P. densus 0.07 0.00 0.00 0.00 ± ± ± ±

P. ®liformis 0.15 0.20 0.00 0.12 0.11±0.30 0.05±0.18 ± ±

P. friesii 0.33 0.23 0.02 0.09 0.11±0.30 0.03±0.15 0.00±0.07 0.00±0.05

P. gramineus 0.15 0.15 0.00 0.17 0.07±0.22 0.10±0.25 ± ±

P. lucens 0.52 0.30 0.03 0.14 0.19±0.41 0.08±0.20 0.00±0.17 0.00±0.06

P. natans 0.74 0.73 0.18 0.52 0.62±0.81 0.43±0.63 0.04±0.33 0.11±0.26

P. obtusifolius 0.26 0.13 0.00 0.46 0.04±0.19 0.35±0.55 ± ±

P. pectinatus 0.48 0.30 0.18 0.62 0.19±0.41 0.53±0.73 0.07±0.33 0.11±0.26

P. perfoliatus 0.59 0.50 0.15 0.49 0.41±0.59 0.38±0.58 0.04±0.30 0.08±0.23

P. polygonifolius 0.04 0.08 0.00 0.00 0.00±0.11 ± ± ±

P. praelongus 0.41 0.13 0.08 0.12 0.04±0.19 0.05±0.18 0.00±0.19 0.03±0.14

P. pusillus 0.33 0.23 0.01 0.49 0.15±0.30 0.40±0.58 0.00±0.07 0.00±0.05

P. rutilus 0.00 0.00 0.00 0.03 ± 0.00±0.05 ± ±

P. zosterifolius 0.56 0.25 0.00 0.08 0.15±0.33 0.03±0.13 0.00±0.04 0.00±0.02

Table 2 Correlations between the frequency of occurrence

of Potamogeton species in lakes or streams in 1896 and

1996. Spearman rank correlation coe�cients (r) are given

with the level of signi®cance in parenthesis

Lakes 1996

Lakes 1896 vs. streams 1896 0.87 (0.001)

Lakes 1896 vs. lakes 1996 0.78 (0.01)

Streams 1896 vs. streams 1996 0.69 (0.01)

Lakes 1996 vs. streams 1996 0.73 (0.01)

1034Macrophyte

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Ecological Society

Journal of Ecology,

88, 1030±1040

the abundance-rank relationship is a measure of

evenness in the distribution, with low slopes

observed at high evenness (Smith & Wilson 1996).

The contemporary stream vegetation has a signi®-

cantly lower evenness than that of either contempor-

ary lakes (t-test for di�erences in slope, t� 4.6, P<

0.05) or old streams (t� 16.3, P<0.01). Evenness

of lake vegetation has also declined signi®cantly

over time (t� 4.4, P<0.05). Evenness was not sig-

ni®cantly di�erent in lakes and streams studied 100

years ago (t� 1.6, P>0.05).

We evaluated whether environmental changes

over time had led to directional changes in the rela-

tive abundance of Potamogeton species by determin-

ing the correlations between their relative

occurrence and morphological indices re¯ecting

eutrophication tolerance and dispersal capacity

(Table 3). We found no systematic changes in the

correlations in lakes; although correlations between

species abundance and local or regional dispersal

capacity had increased, the di�erences were not sig-

ni®cant.

ABUNDANCE-RANGE SIZE RELATIONSHIP

In the contemporary stream ¯ora, mean local abun-

dance was signi®cantly and positively related to geo-

graphical range size of the 57 species found at one

or more of the 208 localities (Fig. 4). Thus, wide-

spread species were also locally abundant, while

some species of a restricted range size were also

locally rare, while others were relatively abundant at

the few localities at which they occurred. There were

no widespread species of a low local abundance

(Fig. 4).

Fig. 3 Rank-abundance diagrams for Potamogeton species in lakes and streams in 1896 (*) and 1996 (W). All regression

lines were highly signi®cant (r2 : 0.87±0.95; P<0.01).

Table 3 Correlations between frequency of occurrence and indices of dispersal and morphology (see text) of Potamogeton

species. Frequency of occurrence is based on studies in 40 lakes and 27 streams in 1896 and 66 lakes and 208 streams in

1996. Spearman rank correlation coe�cients (r) are given with the level of signi®cance in parenthesis. There were no signi®-

cant di�erences between the two surveys in any of the parameters (P>0.05)

Species frequency 1896 Species frequency 1996

Lakes

Dispersal index 0.540 (0.037) 0.510 (0.048)

Regional dispersal 0.550 (0.033) 0.576 (0.026)

Local dispersal 0.379 (0.142) 0.312 (0.227)

Morphology index 0.525 (0.042) 0.451 (0.081)

Floating leaves/rami®cation 0.154 (0.551) 0.229 (0.374)

Plant height 0.628 (0.015) 0.484 (0.061)

Streams

Dispersal index 0.145 (0.574) 0.374 (0.148)

Regional dispersal 0.098 (0.704) 0.380 (0.141)

Local dispersal 0.132 (0.609) 0.229 (0.374)

Morphology index 0.576 (0.026) 0.488 (0.059)

Floating leaves/rami®cation 0.125 (0.629) 0.073 (0.777)

Plant height 0.716 (0.006) 0.663 (0.010)

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Journal of Ecology,

88, 1030±1040

Discussion

CHANGES OF LAKE FLORA

The relationship between the trophic state of lakes

and the species richness of vascular plants is uni-

modal with the maximum number being observed

under mesotrophic conditions. The coarse nutrient-

poor sediments can support small slow-growing spe-

cies either alone or as an understorey below taller,

more nutrient-demanding species (Chambers 1987;

Rùrslett 1991; Vestergaard & Sand-Jensen 2000).

Development of lake vegetation therefore depends

both on the initial nutrient status, and on the extent

of nutrient enrichment. Thus, in Finland the predo-

minantly oligotrophic lakes have become richer in

submerged species following 40 years of eutrophica-

tion (Rintanen 1996), whereas in fertile lowland

regions of Denmark and other parts of Europe

many lakes were already mesotrophic or eutrophic

100 years ago and have su�ered a reduced distribu-

tion and richness of submerged species associated

with greater phytoplankton blooms, and denser

stands of emergent and ¯oating-leaved plants

(Wesenberg-Lund et al. 1917; Christensen &

Andersen 1958; Klein 1993; Odgaard et al. 1997).

Although some Danish lakes have been polluted by

municipal sewage and have thus had little sub-

merged vegetation since medieval times (Klein

1993), most have experienced deterioration of sub-

merged macrophyte populations only over the past

100 years (Fig. 1; Olsen 1964; Odgaard et al. 1997).

Changes of lake vegetation upon eutrophication

are characterized by an early loss of small, slow-

growing vascular rosette species (i.e. isoetids),

mosses and characeans (Roelofs 1983; Arts et al.

1990; Blindow 1992; Sand-Jensen 1997). Six lakes

lost their isoetid communities entirely between the

two surveys (Baagùe & Ravn 1895ÿ96; Iversen

1929; Sand-Jensen 1997; Odgaard 1998; Vestergaard

1998), four isoetid species are now found in fewer

than ®ve sites (Vestergaard 1998) and only Litorella

uni¯ora remains relatively common. Characeans

used to be common in deep-water communities in

transparent, alkaline lakes (Klein 1993; Odgaard

et al. 1997), but 13 species are now restricted to just

a few lakes (Vestergaard 1998).

Potamogeton species have a rather tall growth

form (elodeid form), and this is generally associated

with less dramatic decline (Odgaard et al. 1997;

Sand-Jensen 1997). Species typical of oligotrophic

habitats (e.g. P. alpinus, P. ®liformis and P. polygo-

nifolius) have tended to be replaced by those of

eutrophic habitats (e.g. P. crispus, P. pectinatus and

P. perfoliatus, Newbold & Palmer 1979; Holmes &

Newbold 1984; Preston 1995) in Danish lakes

(Table 1), and evenness has thus declined signi®-

cantly. P. pectinatus has become the most common

submerged species and is often associated with

Ceratophyllum demersum, Elodea canadensis,

Myriophyllum spicatum and P. crispus (Vestergaard

1998), which are similarly fast-growing, nutrient

demanding species capable of forming a dense

canopy below the water surface (Adams &

McCracken 1974; Nichols & Shaw 1986; van der

Bijl et al. 1989).

The morphological indices do not, however, sug-

gest systematic alterations towards greater abun-

dance of Potamogeton species better able to tolerate

eutrophic and turbid waters (Table 3). Insu�cient

knowledge of the autecology of Potamogeton spe-

cies, the crude nature of morphological indices and

the presence of di�erent lakes in the old and con-

temporary studies, however, makes the trend from

eutrophic to oligotrophic species di�cult to evalu-

ate. For example, two small species (P. obtusifolius

and P. pusillus) apparently have a relatively greater

distribution today than 100 years ago, while the

large P. zosterifolius has declined steeply and pre-

sently only holds marginal populations (Table 1,

Vestergaard 1998). Comprehensive recent studies of

lakes, often aided by Scuba diving, make it very

likely that any species declines observed are real,

and may even be underestimated, while species

increases could be artefacts of the production of

more careful inventories, particularly for small,

deep-growing species. The nutrient and light require-

ments of these three species are not known, and the

morphological indices make no allowance for di�er-

ences in resource requirements, intrinsic growth rate

or ability to withstand environmental stresses linked

to eutrophication (e.g. high pH, reduced sediments

and alternating oxygen conditions).

The general pattern is, however, the same as

recorded for the distribution of many individual

Potamogeton species in lakes in England (Preston

1995), Finland (Kurimo 1979; Rintanen 1996) and

The Netherlands (Mesters 1995) with P. alpinus, P.

®liformis, P. lucens, P. polygonifolius, P. praelongus

and P. zosterifolius declining and P. crispus and P.

pectinatus becoming relatively more abundant.

Fig. 4 Mean local abundance as a function of range size of

57 species in 206 stream localities in Denmark. The regres-

sion line was signi®cant (r2� 0.222; P<0.001).

1036Macrophyte

decline in Danish

lakes

# 2000 British

Ecological Society

Journal of Ecology,

88, 1030±1040

Palaeolimnological studies (Klein 1993) suggest that

eutrophication had initiated the decline of P. zosteri-

folius in the 1700s and 1800s. Detailed studies in

Lake Fure during its shift from a transparent meso-

trophic state in the early 1900s to a turbid,

eutrophic state in the 1950s also document a com-

plete loss of isoetids, characeans and mosses, a

decline of small elodeid species and the persistence

of most tall canopy-forming elodeids (Petersen &

Raunkiñr 1917; Christensen & Andersen 1958;

Sand-Jensen 1997). While P. ®liformis and P. zosteri-

folius disappeared early during the eutrophication of

Lake Fure, P. crispus and P. pectinatus have

increased from a low rank among the original 36

submerged species to a high rank among the surviv-

ing 12 species (Sand-Jensen 1997).

CHANGES OF STREAM FLORA AND

SIMILARITIES WITH LAKES

Richness and evenness of Potamogeton species have

declined very markedly in streams. Firstly, physical

disturbance due to channelling, weed cutting and

dredging of sediments has generated a more stan-

dard environment which imposes greater demands

on robustness, growth rate and dispersal capacity of

the plants (Barrat-Segretain 1996; Henry et al. 1996;

Barrat-Segretain et al. 1998). In the past the pre-

sence of ri�es with high ¯ow and coarse sediments

and meanders or backwaters with low ¯ow and ®ne

sediments has facilitated the existence of a diverse

¯ora, even including some species typical of the shel-

tered habitats also found within lakes (Ostenfeld

1913). Secondly, many streams have become pol-

luted by organic wastes and dissolved nutrients lead-

ing to the point where susceptible species su�er

acute toxicity, and die-back due to anoxia and over-

growth by blanketing macroalgae and microbial

communities (Sand-Jensen et al. 1989a,b). Thirdly,

eutrophic, turbid lakes located along the course of

streams have lost their submerged vegetation and

therefore act as a sink for plant dispersal (Riis &

Sand-Jensen 2000) rather than a source for the

export of propagules (Nielsen 1872±76; Baagùe &

Ravn 1895±96; Andersen 1910).

Such environmental changes can account for the

overall decline of species richness in streams, the

loss of many Potamogeton species and the possible

trend towards a relatively greater abundance of spe-

cies with a high dispersal capacity (Table 3; Riis &

Sand-Jensen 2000). Only P. crispus, P. natans, P.

pectinatus and P. perfoliatus have remained relatively

common in streams, and all four are fast-growing

species typical of eutrophic, disturbed environments

(Newbold & Palmer 1979; Grime et al. 1988; Sand-

Jensen et al. 1989b; Nùrgaard 1992). It has been

shown that P. crispus (Nichols & Shaw 1986;

Sabbatini & Murphy 1996), P. pectinatus (Sand-

Jensen et al. 1989b) and P. perfoliatus (Nùrgaard

1992) all respond to cutting through enhanced

regrowth. Oligotrophic species (e.g. P. alpinus and

P. polygonifolius; Newbold & Palmer 1979) and

large, broad-leaved species (e.g. P. lucens, P. prae-

longus and P. zosterifolius) have, in contrast,

declined dramatically in abundance (Table 1). The

importance of management is reinforced by the

lower abundance of large Potamogeton species 100

years ago at sites where manual weed cutting had

just commenced (Baagùe & Ravn 1895ÿ96), and the

richer and spatially more heterogeneous vegetation

today in uncut reaches, compared with neighbour-

ing, regularly cut reaches (Baattrup-Pedersen et al.

1998).

The submerged vegetation in Danish streams

today is typically dominated by Elodea canadensis

and Sparganium emersum and a few robust species of

Ranunculus and Callitriche (Riis et al. 2000). These

species show a high growth capacity and e�cient

dispersal of detached shoots, which are transported

by the current and rapidly develop adventitious

roots but form new monospeci®c stands when

caught on the stream bed (Moeslund et al. 1990;

Kronvang et al. 1994; Sand-Jensen et al. 1999).

It is di�cult to test to what extent aspects of

resource use, resource availability and metapopula-

tion dynamics of dispersal and colonization (e.g.

Gaston et al. 1997) can account for the positive

interspeci®c relationship between local abundance

and range size observed in the contemporary stream

vegetation. Several factors suggest, however, that

metapopulation dynamics are particularly important

for the stream vegetation. Streams are naturally

very perturbed due to the frequent changes in velo-

city which lead to the loss of plant stands and sedi-

ment erosion and thus result in unvegetated stream

beds, and disturbance has been further enhanced by

human impact (particularly weed cutting and dred-

ging; Madsen 1995). In addition, many stream

plants are e�ectively dispersed via turions and

detached shoots which are capable of rooting and

then forming new stands through fast clonal growth

(Barrat-Segretain et al. 1998; Sand-Jensen et al.

1999). Dispersal is enhanced by the longitudinal

connectance within stream systems and the proxi-

mity to permanent semi-aquatic populations close to

the shore (Henry & Amoros 1996).

This frequent decline, redistribution and recoloni-

zation of the plant stands would be expected to pro-

mote a strong positive relationship between local

abundance and range size in the stream commu-

nities, similar to that observed in terrestrial commu-

nities of herbaceous plants in wheat ®elds, Brassica

®elds and fallow arable land (Thompson et al.

1998). There are larger dispersal barriers between

separate stream systems than between individual

sites within a system. The positive interspeci®c rela-

tionship is therefore even stronger among such sites

1037K. Sand-Jensen

et al.

# 2000 British

Ecological Society

Journal of Ecology,

88, 1030±1040

(data not shown) than that presented for a range of

systems with a number of di�erent dominant spe-

cies.

FUTURE DEVELOPMENT OF THE AQUATIC

FLORA

The aquatic ¯ora presently includes a large propor-

tion of rare species. In streams such species vary in

abundance at the few localities where they occur

(Fig. 4). Rare aquatic plants in Denmark, include

®ve species of Potamogeton (P. acutifolius, P. colour-

atus, P. densus, P. rutilus and P. zosterifolius), four

isoetids and 10±15 other vascular species (Moeslund

et al. 1990; Vestergaard 1998; Riis & Sand-Jensen

2000) and many of these are also threatened in

other European countries, appearing in national and

international Red-lists (Preston & Croft 1997).

Some species with a solely European distribution

(e.g. Luronium natans, Oenanthe ¯uviatilis and

Potamogeton acutifolius) face the risk of going

extinct, while many others hold only marginal popu-

lations and will therefore have di�culty colonizing

newly suitable habitats generated through improved

water puri®cation, restoration of lakes and re-estab-

lishment of meandering streams (Iversen et al.

1993). The physico-chemical quality of streams, and

in some cases lakes, can be restored, but the possibi-

lity and time scale of recovery of the former diver-

sity of submerged species is unknown. Robust

species have monopolized the environment and

these may resist the spread and regrowth of rare

species, hampering recolonization from marginal

populations.

The landscape of European lowland countries is

increasingly fragmented and subject to continuous

disturbance by natural and anthropogenic events

(Bobbink et al. 1998; Bradshaw & Holmqvist 1999).

The extent to which communities can be reconsti-

tuted under suitable conditions must be related to

species traits, population size and the proximity of

potential colonisers (Grime 1998). Freshwater habi-

tats suitable for submerged plants have been parti-

cularly eroded, and coupled with the decline in

population sizes will make re-assembly of aquatic

communities even more di�cult.

Acknowledgements

We thank the Danish Natural Science Research

Council (grant 11±7795) and the Danish Research

Academy for ®nancial support. We thank Bent

Odgaard and Anne Garde for helpful comments on

the manuscript.

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