KM
Hydrobiologia 524: 145-156. 2004.
145
B9 © 2004 Khtwer Academic Publishers. Printed in the Netherlands.
A century of change in macrophyte abundance and composition in response to
agricultural eutrophication
Christopher J. Egertson1'2, Jeff A. Kopaska1'3 & John A. Downing1*
^Ecology, Evolution, and Organismal Biology, Iowa State University, 353 Bessey Hall, Ames, IA 50011-1020, USA
2Present address: Oregon Natural Desert Association, 16 N.W. Kansas Avenue, Bend, OR 97701, USA
3Present address: Iowa Department of Natural Resources, 1436 255th Street, Boone, IA 50036, USA
(* Author for correspondence: E-mail: downing@iastate.edu)
Received 25 April 2003; in revised form 15 January; accepted 19 January 2004
Key words: macrophytes, long-term, eutrophication, phosphorus, water clarity, lake
Abstract
Clear Lake, Iowa, USA is a shallow, agriculturally eutrophic lake that has changed drastically over the past
century. Eight macrophyte surveys since 1896 were pooled and examined to characterize long-term impacts
of eutrophication on macrophyte community composition and relative abundance. Surveys in 1981 and
2000 revealed few submergent and floating-leaved species and a dominance in emergent species (Scirpus,
Typha). Over the past century, however, species richness has declined from a high of 30 species in 1951 to 12
found today, while the community composition has shifted from submergent- (99%) to emergent-domi
nated floras (84%). Potamogeton praelongus was the first emergent species to disappear but was followed by
several other clear water Potamogeton species. Several floating leaved and emergent genera increased in
relative abundance with eutrophication, notably Nuphar, Nymphaea, Phragmites, Polygonum, Sagittaria,
Scirpus, and Typha. P. pectinatus was present over the entire century due to its tolerance of eutrophic
conditions. Macrophyte growth was generally light-limited, with 93% of the variance in relative abundance
of submergent species explained by changes in water transparency. Clear Lake exhibits signs of alternative
stable states, oscillating between clear and turbid water, coupled with high and low submerged species
relative abundance. The maximum macrophyte richness occurred as the lake oscillated between submer
gent- and emergent-dominated states. Changes in the water level have also impacted macrophyte growth
since the area of the lake occupied by emergent macrophytes was negatively correlated with water level.
Strongest correlations indicated that macrophytes respond to water level variations with a 2-year time-lag.
Introduction
Aquatic macrophytes, key components of aquatic
column through uptake (Goulder 1969; Van donk
ecosystems, are impacted by eutrophication, yet
they provide a buffer against water quality degra
et al., 1993; Kufel & Ozimek, 1994).
dation. They offer habitat and food for aquatic
tible to anthropogenic alteration, eutrophied by
organisms (Timms & Moss, 1984; Engel, 1988;
increased nutrient and sediment loads and altered
Over their histories, shallow lakes are suscep
Venugopal & Winfield, 1993), decrease the con
hydrology. Aquatic macrophyte communities can
centration of suspended solids in the water column
be influenced by these changes in nutrient levels
(Van den Berg et al., 1997; Barko & James, 1998),
and
and lower concentrations of nutrients in the water
richness has been observed to decrease as lakes
physical
conditions.
Macrophyte
species
146
eutrophy (Niemeier & Hubert, 1986; Sand-Jensen,
1997) due to light limitation to submerged vegeta
tion (Scheffer et al., 1992; Skubinna et al., 1995).
As water transparency declines, macrophyte com
munities can shift in composition from a domi
nance
of
submergent
(e.g.,
Cham
spp.),
to
canopy forming (e.g., Potamogeton spp.), to float
ing-leaved
(e.g.,
Nuphar spp.),
and
to
emer
2002) and permit photosynthetically active radia
tion to penetrate to new areas in the water column
(Chambers & Kalff, 1985). Both can lead to altered
growth and distribution of macrophyte species
(Wallsten & Forsgren, 1989; Blidnow, 1992; Gafny
& Gasith, 1999).
Because anthropogenic eutrophication has oc
curred over a great time period, long-term data are
gent vegetation (e.g., Scirpus spp. and Typha spp.)
essential to an understanding of the trajectory of
(Niemeier
riched and can trigger a switch from a clear-water
changes in macrophyte communities. Only longterm data can reveal trends that exceed the subdecade scale (Magnuson et al., 1991). Long-term
data on lake ecosystems, especially those predating
anthropogenic influences, are very rare (Sand-
to a turbid-water stable state (Scheffer,
&
Hubert,
1984;
Chambers,
1987;
Moss, 1988; Sand-Jensen, 1997; Van Den Berg,
1999). Such changes lead to decreased abundance
and diversity of macrophytes as lakes become en
1990).
Jensen, 1997), making such records particularly
Lakes in turbid stable states have often shifted
valuable. Here we extend the span of study of
from submergent species dominance and clear
macrophytes in Clear Lake (c.f., Niemeier & Hu
water to emergent species dominance with high
bert,
turbidity. They also have discernible feedback
lake (Fig. 1).
mechanisms (e.g., nutrients, waves, carp) sustain
1986), an agriculturally impacted shallow
Clear Lake has undergone significant changes
ing the longevity of the turbid state Scheffer et al.,
in water quality and watershed characteristics over
2002).
the last century. Water transparency has decreased
Another factor that can mediate the dominance
from at least 1.5 m in 1896 to 0.4 m in 2000, while
and structure of macrophyte communities is water
phosphorus concentrations have increased from
anthropogenic
<20 /ig P1 in 1934 to 190 ng I"1 in 2000 (Fig. 2).
modulation of hydrology. As water level decreases,
Its small watershed has changed from forest, tall
grass prairie, and oak savannah to 60% farm land,
level
alteration
resulting
from
macrophytes may overcome light limitation. Light
can reach the sediment and germinate seeds (van
10% urban, and 10% pasture (Downing et al.,
der Valk, 1978; Medeiros dos Santos & Esteves,
2001). Because Clear Lake is shallow (Z, 2.9 m;
Clear Lakejowa, USA
^ Farm land
^ Urban & residential
«■ Grass & pasture
ra Wetland
m Forest
5 km
Figure I. Map of Clear Lake, Iowa, USA and its watershed showing landuse.
147
rophyte and water quality information date back
(a)
()
O
160 -
/
•
3
120 -
CO
o
80 •
/
/
/
o
Q.
40 -
0 -
P< 0.02
aquatic macro-
i
* •
(b)
sons,
i
large
iVjt
0.4 -
1880
1958;
emergent
macrophyte
beds
because
an
of sediment at random locations, determined
that <1% of submerged macrophytes were located
outside these ten emergent beds. Each bed
was intensively surveyed using methods similar
to Niemeier & Hubert (1984). To estimate species
N TV>
i- 0.43
P< 0.01
Riddenhour,
extensive preliminary survey, employing raking
0)
(0
a.
1952;
July 2000. We concentrated our analysis on ten
f
i
Pearcy,
ek, 1896) and a new intensive survey performed in
j
0.8 -
1950;
Mrachek, 1966; Niemeier & Hubert, 1984; Shim-
t
1.2 -
Methods
lished literature (Bailey & Harrison, 1945; Par
r
0 -
on
sition and species relative abundance, aquatic
8
c
eutrophication
macrophyte data were collected from the pub
/
E
JC
agricultural
phytes in shallow lake ecosystems.
In order to assess changes in community compo
o
•i fi
l.O
further elucidate and document the impact of
Cf
5
a.
as far as 1896. A long-term study of this nature can
occurrence, we placed a 1-m2 quadrat every 20 m
along transects perpendicular from the shore
to the outer limit of the macrophyte beds. Tran
sects were situated every 20 m along the shoreline.
1*1
1920
1960
Year
2000
Figure 2. Historical changes in phosphorus (/ig 1 ') (a) and
water transparency (Secchi disc; m) (b) since 1896 and 1934,
respectively. Solid lines represent least squares trends, broken
line represents a time trend. Filled symbols indicate inorganic
phosphorus concentrations and open symbols indicate total
phosphorus concentrations. Sources of data listed in Methods.
The r2 and p are the coefficient of determination and the
probability of obtaining this r2 by chance alone.
To generate the most comprehensive species
list possible, species observed along transects,
outside of the quadrats, were also noted. Voucher
specimens of each species found were collected
and identified using Fassett (1940) and were
deposited in the Ada Hayden Herbarium of
the Department of Ecology, Evolution, and
Organismal Biology (353 Bessey Hall, Iowa
State University, Ames, IA 50011). Water depth
and substrate type were noted at each sam
pling location.
Zmax* 5.9 m) and turbid, interannual variation in
water level may also play a role in the areal dis
tribution and composition of macrophyte com
All macrophytes were identified to the species
level except Scirpus and Typha. These were only
identified to genus because hybridization between
S. validus and S. acutus and between T. augusti-
munities.
folia and T. latifolia (i.e., T. glauca) are prevalent
The purpose of this analysis was to examine
in the lake (Niemeier & Hubert, 1984). Scirpus and
changes in macrophyte community composition
Typha species found in this and previous studies
and species occurrence with water quality and
were therefore grouped into Scirpus and Typha
spp. categories.
water level changes over the past century. This
historically popular recreational lake offers a rare
long-term record for North America since mac
Macrophyte relative abundances were quanti
fied based on percent frequency of occurrence in
148
examined quadrats. Taxa were classified as rare
Small (1961), United States Environmental Pro
(<0.25% of quadrats), occasional (0.26-1% of
quadrats), common (1-5% of quadrats), abundant
(5-20% of quadrats), and very abundant (>20% of
tection Agency (1976), Bachmann (1980, 1994),
Crumpton
quadrats; Niemeier & Hubert, 1986). Although
only Niemeier & Hubert's (1984) and our new
are inorganic phosphorus (determined by the
stannous chloride method), while later dates,
(1994,
unpublished),
and
Downing
et al. (2001). Concentrations from 1934 and 1961
study were fully quantitative, all other studies
1974-2000, are expressed as total phosphorus
indicated relative abundances as rare, occasional,
(determined by the ascorbic acid method). The two
common, abundant, or very abundant We con
inorganic concentrations are probably somewhat
verted
these
categorical
indicators
of relative
inaccurate because of the difficulty in replicating
abundance to the medians of the ranges noted
concentrations using the stannous chloride method
above as deduced by Niemeier & Hubert (1986).
(Murphy & Riley, 1962).
Relative abundance estimates for each functional
Water transparency data measured by Secchi
group (e.g., submergent or Rs, floating leaved or
disk depth were collected from Shimek (1896),
Rf, emergent or Rq) were calculated for each survey
Neal (1962), United States Environmental Pro
by summing the median score for all taxa in each
tection Agency (1976), Bachmann (1980, 1994),
functional group after Fasset (1940). We were then
Crumpton (1994, unpublished), and Downing et
able to gauge historical trends of i?s, /fo and Rc by
al. (2001). The datum from Shimek (1896) was
expressing their sum (RK) as the fraction of the
estimated from field notes describing Potamogeton
total sum of all scores for all taxa documented in
praelongus as >3 m long. This indicates that Sec
each survey (RJY,R)- Simple temporal trends in
chi depth was at least 1.5 m at the time because
relative abundances of individual species and taxa
submerged macrophytes can only grow to 2-3
were assessed by converting the relative abun
times the Secchi depth (Canfield et al.,
dances to numerical scores of 0-6 (for absent,
Chambers & Kalff, 1985).
1985;
present, rare, occasional, common, abundant, very
abundant, respectively) and applying Pearson's
correlation analysis across years (Snedecor and
Results
Cochran, 1989).
Since water level can impact macrophyte dis
Over 500 quadrats sampled in 2000 collected a
tribution and composition, we compared the area
total of 12 species of macrophytes. These included
of emergent beds (ha) and Rs, Rf, and i^e data in
four emergent taxa (Typha spp., Scirpus spp.,
concert with yearly water level (m) averages. Wa
Sagittaria
ter level data were obtained from the United States
floating-leaved species (Nuphar advena, Nymphaea
latifolia,
Phragmites
australis),
two
Geological Survey National Water Information
tuberosd), and six submergent taxa {Potamogeton
System web database (http://waterdata.usgs.gov/
nodosus, Potamogeton pectinatus, Ceratophyllum
nwis/). Emergent bed area was estimated by digi
demersum, Vallisneria americana, Chara sp., Pot
tizing aerial photographs taken by the Farm Ser
amogeton crispus; Fig. 3). Our survey showed that
vice Agency (Mason City and Garner, IA, USA) in
macrophytes
years 1979-2000 and a macrophyte cover map
approximately 1% of the total lake surface area
lands, CA, USA). Because the impact of water
surveyed were located on silt/sand sediment and in
level on vegetation may have a lag-time in its
<1 m of water. The emergent genera Scirpus and
(Pearcy, 1952) using Arcview 3.2® (ESRI, Red-
covered
19 ha,
accounting
for
1468 ha). All ten beds of emergent vegetation
influence on macrophyte growth (van der Valk,
Typha were most abundant followed by Pota
1980; Mitsch & Gosselink, 2000), we compared
mogeton
macrophyte data with data on yearly averaged
tuberosa, and Potamogeton pectinatus (Fig. 3). All
water level from the year of estimation of macro
other species occurred in <0.1% of the quadrats
phyte cover as well as water levels over the previ
sampled.
ous 3 years.
Organic and inorganic phosphorus (ng I"1)
data were gathered from Bailey & Harrison (1945),
nodosus,
Nuphar
advena,
Nymphaea
Since 1981, species richness in Clear Lake has
declined from 20 to
12 species (Table 1). We
found, as did Niemeier & Hubert (1984), that
149
Taxon
1896
1944
1950
■
Chara sp.
Najasjlexilis
1952
1
Hij
1
HI
1
1
1
I
■
1
HH
Poiamogeton alpinus
Poiamogeton amplifolius
|
Potamogelon friesii
|
Potamogelon illinoensis
Potamogelon natans
d
«
8?
^^
Potamogeton nodosus
Poiamogeton pectinatus
|
Poiamogeton praelongus
H
Potamogeton pusillus
|
Poiamogeton rishardsonii
Potamogeton zosteriformis
^|
|H
I
1
H
^H
1
IH
1958
1966
HH
■
HI
Hi
^H
H
H
■
I^H
■
■
■
H
1984
2000
1
1
H
H
I
H
i
Poiamogeton crispus
I
Zannichetlia palustris
Elodea canadensis
Vallisneria americana
m
|^H
I
I
Heteranthera dubia
IHI
Ceratophyllum demersum
Myriophyllum hcterophyllum
Myriophyllum exalbesccns
1
■
■
1
i
^^|
H|
I
1
■
Myriophyllum sp.
Ulricularia vulgaris
1
■
i
Lemna minor
I
Spirodela polyrhha
■
Woljjia Columbians
«
w
E
■
■
■
■
Polygonum ampltibium
Polygonum coccineum
Polygonum lapathigolium
1
1
1
1
Polygonum punctntum
hi
Nuphar advena
Nymphaea tuberosa
■
1
H
■
1
I
H
■
H
Alisma plantago aquatica
■
Sagittaria latifolia
Sagittaria rigida
1
1
Sagittaria teres
Carex comosa
■a
B
M
1
I
I
Cartx hystricina
■
Cyperusferruginescens
Cyperus sp.
Eleocharis acicularis
w Eleocharis palustris
HH
Scirpus spp.
Sparganium eurycarpum
HH
1
Echinochloa pungens
Phragmites australis
1
H
1
■
^H
HI
I
1
1
1
Bidens cernua
■
Bidens connaiu
va
p
va
p
va
p
I
1
Equiseiumfluviatile
p
1
v(
p
va
p
va
p
va
p
va
Figure 3. Species found in each functional group (submergent. floating, emergent) and their relative abundance in each of eight
macrophyte surveys dating back to 1896. Relative abundance was determined from the fraction of total quadrats containing species.
Bars indicate macrophyte relative abundance and follows the scale at the bottom of the figure representing macrophytes being present
to 'very abundant'. Scale indicates/? for 'present', but no abundance information; rare (<0.25% of quadrats); occasional (0.26-1% of
quadrats); common (1-5% of quadrats), abundant (5-20% of quadrats); va is for very abundant (>20% of quadrats). Data sources are
listed in the Methods section.
emergent genera Scirpus and Typha were the most
species were few and rare respectively (Fig. 3). The
prevalent,
nine common
and
floating-leaved
and
submergent
species to both
studies showed
150
100
100
□ Emergent
■ Floating
Submergenl
Figure 4. Fraction oi quadrats containing each of nine com
mon species in surveys performed in 1981 and 20011. Nole the
scale break between common (emergent) and less common
1920
(floating-leaved and submergenl) species.
Year
1960
2000
Figure 5. Long-term trends of the percent relative abundance
{RjYlR) of functional groups, submergenl (#s), floating-leaved
general similarities in occurrences over the past
(R,), und emergent macrophytes (Rc). between I896 and 2(100.
two decades (Fig. 4).
'VR is the sum of !<„ R, and RL. while 8, represent one of the
Species richness and composition have both
three functional groups. Me;ins of calculation of percent rela
tive abundance for each functional group from historical data is
changed radically over the last century. Species
explained in the Methods section.
richness decreased from a high of 30 species (Pe-
arcy, 1952) to 12 species found in 2000 (Table 1).
Species composition changed in dominance from
some Typha spp. Today Scirpus and Typha are the
primarily submergent to mostly emergent species
most abundant genera in Clear Lake, with Typha
(Fig. 5). Submergent macrophytes made up nearly
having expanded greatly since 1951.
100% of the flora in 18%, but were reduced to less
than 5% of the species found in 2000. Floating-
Some species disappeared as
eutrophication
progressed while others appeared as water quality
leaved species remained fairly constant across the
changed (Fig. 3). For example, Potamogetonprae-
century at <5% of the species, but became rela
longus, common in the late 1800s. declined signif
tively more abundant in 2000 (>10%). as general
species richness
creased from
declined.
<\% to
Emergent
species
icantly (Table 2) and was not found in the lake
in
after IS96. Several other species of Potamogeion
>80% of the macrophyte
also
species. Shimek (1896) reported no Scirpus spp. or
declined
P. friesii,
P.
significantly with
zostertformis,
P.
time,
including
ampHfolius,
and
Typha spp. in the lake, but by 1951, Pearcy (1952)
P. natans. Other species showing temporal declines
reported large-conspicuous Scirpus spp. beds and
were
Myriophyllum
heterophyllunt,
I'allisncria
Table I. Species totals and relative abundance for submergent {R.,), iloaling-leaved (flr), and emergent [J?J species
1896
1945
1950
1952
1958
1966
I9S4
2000
14
i 1
24
30
11
24
20
12
11 5
58
21
93
60
46
2
3
Floating-leaved relative abundance {R-)
5
5
0.1
7
0
6
6
Emergent relative abundance (fiL.)
D
23
20
60
6
24
40
Species total
Submergent relative abundance (/?,)
40
See Methods section for means of calculation of relative abundance from historical data. Fxcept for this study (2000), years indicate
when macrophyte data were published. Data sources are Shimek (1896); Bailey & Harrison (1945); Parsons (1950); Pearcy (1952)
Riddenhour(l95S): Mrachek (1966); Niemeier & Hubert )I9S4); and this study.
151
Table 2. Temporal correlations between the relative abundance of the taxa in Figure 3 and the year of observation
Taxon
P
r
Last year observed
First year observed
(declining species)
(increasing species)
Potamogeton praelongus
-0.79
0.01
1896
Potamogeton friesii
-0.79
0.02
1896
Potamogeton zosteriformis
-0.79
0.02
1896
Myriophyllum heterophyllum
-0.79
0.02
1896
Eloclea canadensis
-0.76
0.03
1966
Potamogeton amplifolius
-0.74
0.04
1952
Vafiisneria americana
-0.67
0.07
2000
Potamogeton natans
-0.63
0.09
1966
Myriophyllum exalbescen
-0.63
0.09
1966
Potamogeton richardsonii
-0.62
0.10
1966
Nuphar advena
0.69
0.06
1950
Typha spp.
0.72
0.04
1944
Scripus spp.
0.78
0.02
1944
The relative abundance scale indicated on Figure 3 was converted to a numerical score where the length of the bars was exchanged for
a scale of 0-6(0 = absent, 1 = present, 2 = rare, 3 = occasional, etc.). Correlations (r) and probabilities of obtaining a greater r by
chance alone (/>), were determined using Pearson's correlation coeflficientt (Snedecor and Cochran, 1989). Only trends with p < 0.10 are
reported here.
americana, and M. exalbescens. Most of these
Because a great deal of variation in Rs was
species disappeared before 1966 (Table 2). Several
explained by transparency, and transparency
alternated between clear-water (>0.8 m Secchi;
e.g., 1896, 1951, 1975) and turbid-water (<0.5 m
Secchi; e.g., 1949, 1965, 1981, 2000) periods
species, notably a few submergents, some floating
leaved species and several emergents became more
prominent after 1950 (Fig. 3). The submergents
P. illinoensis, P. nodosus, Zannichellia palustris and
Heteranthera dubia were not found prior to 1950
but were seen in more than one subsequent survey,
although H. dubia and Z. palustris disappeared
again before 1984. The principal floating leaved
plants before 1950 were Wolffia columbiana and
Lemna minor but Polygonum spp., Nuphar and
Nymphaea have become common since that time.
Further, Sagittaria spp., Eleocharis acicularis and
Phragmites also appeared in later surveys. The
principal genera that became significantly more
Typha, and
Scirpus (Table 2). The only species that was con
common with time were Nuphar,
sistently common throughout the century of study
was Potamogeton pectinatus (Fig. 3).
Because of great changes in water transparency
(Fig. 2(b)) and macrophyte community composi
tion (Fig. 5), we sought to examine the strength of
correlations between Rs, Rf, and Re and water
clarity. Rs was positively correlated with trans
parency (r = 0.93; p < 0.01; Fig. 6), while nei
ther R? nor Re were significantly correlated with
water clarity.
0
0.4
0.8
1.2
Transparency (Secchi; m)
1.6
Figure 6. Relationship between relative abundance of sub
merged species (Rs) and water transparency (m). See Methods
for means of calculations of /?s from historical occurrence data.
The r and probability are the coefficient of determination and
the probability of obtaining this r by chance alone.
152
80
CO
(D
3
cr
60 -
CO
a>
CO
a
xa 40
c3
"c
Q)
0)
CD
,,«
(I)
E 20 H
HI
1980
1985
1990
Year
1995
2000
Figure 7. Historical trend in water level (broken line) and
0.4
emergent macrophyte bed area (solid line). Points indicate years
emergent bed area was measured. Water level data were ob
tained from the USGS and emergent macrophyte bed area was
determined by digitizing aerial photographs (see Methods sec
tion).
0.8
1.2
1.6
Water level
(m; time-lag of two yr)
Figure 8. Relationship
between
area
covered
by
emergent
macrophyte beds and a 2-year lag in water level. Least squares
regression determined that emergent bed area decreased.
(Fig. 2(b)), we examined the historical data to
determine whether Rs also fluctuated among clearand turbid-water periods. Although few studies
offered quantitative data, anecdotal evidence sug
gested that at least one switch occurred between
clear water with abundant submerged plants and
turbid water with few submerged plants. Parsons
(1950) reported that submerged macrophytes were
so abundant in 1945-1946 that boating was nearly
impossible. By 1949, submerged macrophytes had
declined from an R& of 58 in 1944 to only 21
(Table 1), with a concurrent low water transpar
ency of 0.4m (Fig. 2(b)). Three years later, sub
merged plants were abundant (Rs = 93; Table 1)
and
water
transparency
increased
to
1.5 m
(Fig. 2(b)).
The area covered by emergent macrophyte beds
increased as water level decreased (Fig. 7). There
appeared to be a time-lag in response of emergent
bed area to water level changes because bed area
and water level from the same year were not cor
related (p > 0.05), while water level from one,
two, and three years previous to emergent bed area
Table 3. Relationships between yearly averaged water level (m)
data and emergent bed area (ha) data showing a lime-lag
between water level changes and emergent bed area
Yearly averages of water level data
n
r
estimation showed significant (p < 0.05) negative
correlations (Table 3). The best correlation was
provided by a time-lag of 2 years (r2 = 0.46;
p
simultaneous
22
0.17
>0.05
1 y previous bed area estimation
22
0.37
<0.003
2 y previous bed area estimation
22
0.46
<0.00l
3 y previous bed area estimation
22
0.22
<0.05
Emergent bed area data, determined by aerial photographs,
p < 0.001;
Fig. 8). The relative abundance of
macrophyte functional groups (i.e., Rs, Rf and Rc)
did not show any distinguishable trends with water
level (correlation p > 0.05).
Discussion
were compared to water level data, obtained from USGS web
site (http://waterdata.usgs.gov/nwis/), from simultaneous 1, 2,
and 3 yr previous to emergent bed area estimation. Number of
data points is indicated by n, while are r2 and p are the
Agriculturally driven eutrophication has had a
profound impact on the macrophyte abundance
coefficient of determination and the probability of obtaining
and community composition in Clear Lake. Our
this r2 by chance alone.
finding
that
macrophyte communities changed
153
systematically from a dominance of submergent,
increasing
eutrophication,
to floating-leaved, and to emergent macrophytes
Nymphaea,
Phragmites,
as eutrophication increased agrees with the find
Scirpus, and Typha (Table 2; Fig. 3). These genera
observed
to
Nuphar,
Sagittaria,
ings of previous studies (e.g., Kowalcweski &
have frequently
Ozimek, 1993; Sand-Jensen, 1997). Light limita
tion is the most likely explanation for the changes
dominance as eutrophication progresses (e.g., Arts
in macrophyte composition and relative abun
Bertness et al., 2002; Germ et al., 2003). P. pec-
et al.,
been
notably
Polygonum,
increase in
1990; Vaithiyanathan & Richards, 1999;
dance that we observed (Fig. 6). As turbidity in
tinatus was one of the few taxa that remained
creases
no
present throughout the century of water quality
longer penetrate the water column to depths that
decline. This is characteristic of its high tolerance
allow submerged macrophytes to become abun
for eutrophic conditions (e.g., Grassmuck et al.,
through
eutrophication,
light
can
dant (Chambers and Kalff, 1985). Because float
1995) that it attains by forming a canopy to exploit
ing-leaved and emergent species can rely on energy
light near the water surface (Van den Berg et al.,
from rhizomes for short time-spans (Borman et al.,
1999).
1997), they can escape short-term light limitation
and survive impacts of turbidity. Another expla
Clear Lake may have reached the turbid stable
state. This is suggested by the similarity of species
nation for the pattern we observed may be that
relative
submergent macrophytes are unable to root in
(Fig. 4), and the low and stable transparency over
abundances
between
1981
and
2000
loose detritus and silt (Scheffer, 1998; Gafny &
the past few decades (Fig. 2(b)). Patterns of Clear
Gasith, 1999), prevalent in eutrophic lakes. In
Lake vegetation
creased phytoplankton densities can also out-
patterns found in other lakes exhibiting stable
compete macrophytes because phytoplankton can
states (Scheffer et al., 2002). For example, re
decrease
peated oscillations between submergent species
the
availability
of
dissolved
carbon
are consistent with historical
dioxide (Moss, 1990). Mechanical perturbations
dominance during periods of clear water and
by benthivorous fish, e.g., carp (Cyprinus carpio),
emergent species dominance during periods of
and wave action from wind and boats can also
high turbidity between 1945 and 1960 are typical
decrease the success of submergent macrophytes.
of lakes changing among alternative stable states.
Carp, prevalent in eutrophic lakes in this region
Ironically, the maximum taxonomic richness was
(Egertson & Downing, in preparation), and wave
found during this period as the lake oscillated
action can uproot vegetation (Crivelli, 1983; Van
ance also agree with knowledge of the biology and
between submergent- and emergent-dominance.
Current stable turbid conditions and emergent
dominated vegetation may be maintained by
negative feedback mechanisms such as turbidity,
wind, and carp. The ability of this lake to main
tain a stable, clear-water state seems to have been
ecology of aquatic macrophytes. The most strik
compromised by shifts in community composition
ing loss was the early disappearance of P. pra-
accompanying the process of hyper-eutrophication.
Wijk, 1988) and decrease water transparency by
increasing suspended solids (Breukelaar et al.,
1994; Anthony & Downing, 2003).
Patterns of species appearance and disappear
elongus. This species is known to occupy clear
waters
slow-growing.
We found few submergent or floating-leaved
Therefore, other long-term studies have observed
because it
is
large
and
species outside of emergent macrophyte beds.
large declines in this species with eutrophication
Emergent macrophytes can increase water clarity
(Rintanen, 1996; Sand-Jensen et al., 2000). Other
(Dieter, 1990; Horpilla & Nurminen, 2001) possi
disappeared by the end of the study, e.g.,
Potamogeton species that declined over time or
P.
fish perturbations. Therefore, emergent beds may
amplifolius, P. freisii, P. natans, P. pusilis, P. ri-
act as refuges for the few remaining submerged
chardsonii, and P. zosteriformis (Table 2; Fig. 3),
and floating-leaved species.
bly by decreasing wave action and benthivorous
seem to be characteristic of fairly clear waters and
Time-lags appear to be important in responses
have frequently been found in habitats with P.
of emergent macrophyte beds to environmental
change (Fig. 8). For example, as water level de
creases, more surface area of the sediment is
praelongus (Pip, 1987). Several floating leaved and
emergent genera increased
in
abundance
with
154
exposed to light, which may allow for greater
lowing agricultural development. It then began to
germination of seeds (van der Valk, 1978; Medei-
oscillate for 15-20 years before stabilizing in its
ros dos Santos & Esteves, 2002). Under high water
current turbid-water condition.
conditions, however, emergent macrophyte distri
butions likely decrease due to lack of germination,
The history of the aquatic flora in Clear Lake is
one characterized by a systematic decline in sub
anoxic conditions, and perturbation by muskrats
mergent biodiversity and cover. Many species have
(Ondatra zibethicus) (van der Valk, 1980; Froend
vanished and will not likely return without long-
McComb, 1994). Time-lags in macrophyte cover
term, significant, water quality remediation. Be
responses to water-level changes probably reflect
cause this lake is shallow, eutrophic, and has a
the amount of time it takes for germinated seeds to
high likelihood of perturbation from waves and
give rise to substantial root and vegetative mass
benthivorous fish, significant improvement in the
and to depletion of energy stored in rhizomes once
littoral habitat will require long-term, substantial
water level is increased (Mitsch &
changes in transparency, the sedimentary envi
Gosselink,
ronment, and bioturbation.
2000).
Correlations between R^ Rr and Rc and water
level were not statistically significant. This result
differs from Hamabata & Kobayashi's (2002) data
Acknowledgements
indicating an increase in submerged macrophytes
with decreased water level. We may not have been
able to detect correlations between Rs, Rf, and Re
and water level because the range in water level
changes was small (<0.5 m). However, it is possi
ble that because this lake is so shallow, any de
crease in water level may allow macrophytes to
receive a detrimental amount of photosynthetic
radiation, subsequently diminishing macrophyte
biomass (Gafny & Gasith, 1999).
We would like to thank members of the Iowa State
University
Limnology
Laboratory
James
An
thony, Laura Schrage, Nicole Eckles, and David
Knoll for their help and support throughout this
project. A special thanks goes to Rebecca Anthony
who persevered a full day in the field after having
been attacked by a muskrat with a serious attitude
problem. This project was funded by the Iowa
Department of Natural Resources, the city of
Clear Lake, Cerro Gordo County, and Hancock
County.
Conclusions
Long-term, historical observations permitted the
detection of patterns that would not be detected on
shorter time-scales. Our analyses indicated that
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