Hydmbiologia 511: 215-231,2004.
215
© 2004 Kluwer Academic Publishers. Printed in the Netherlands.
Pathways of increased water clarity after fish removal from Ventura
Marsh; a shallow, eutrophic wetland
Laura J. Schrage1-2 & John A. Downing1'*
1 Ecology, Evolution, and Organismal Biology, Iowa State University, 353 Bessey Hall, Ames,
IA 50011-1020, U.S.A.
E-mail: [email protected]
1Present address: Environmental and Public Health Program, University of Wisconsin - Eau Claire,
Eait Claire, WI54702, U.S.A.
(*A uthorfor correspondence)
Received 27 August 2001; in revised form 13 October 2003; accepted 30 October 2003
Key words: biomanipulation, carp, eutrophication, fish, macrophytes, phosphorus, water clarity, wetland
Abstract
We investigated the pathways by which water clarity increases following fish removal by evaluating the effects
of a benthivorous fish reduction in a large, shallow, eutrophic, wetland in a predominately agricultural watershed
in Iowa, U.S.A. Phytoplankton was phosphorus limited prior to manipulation. After a substantial fish removal
was obtained, water clarity increased as a result of decreased suspended sediment and phytoplankton biomass.
Trophic cascading, mitigated by release from fish predation and decreased physical interference from suspended
sediments, appears to determine water clarity. Inorganic suspended solids declined immediately after fish were
removed but the biomass of Daphnia and Ceriodaphnia did not increase until a few weeks after fish removal.
High grazing by zooplankton likely reduced phytoplankton biomass during the height of the clear-water phase.
Phytoplankton appeared to be limited by zooplankton grazing for approximately two months before reverting to
bottom-up control. An increase in suspended sediment and/or increased predation pressure on zooplankton, due to
the return of juvenile carp, appears to account for the decline of larger-bodied zooplankters and the switch back to
bottom-up control. Macrophyte diversity and density increased substantially after the initiation of the clear-water
phase.
Introduction
terest, especially in lakes receiving excessive nutrients
(Lathrop et al., 2002).
Biomanipulation is a well known ecological manage
Despite much study, there remain discrepancies
ment tool aimed at increasing water clarity by ma
concerning the mechanisms of water clarity increase
nipulating the biomass of fish (Hrbacek et al., 1961;
following fish removal. The most commonly cited
Perrow et al., 1997; review by Lathrop et al., 2002).
mechanism is trophic cascading whereby decreased
Biomanipulations have been conducted throughout
fish abundance allows increased zooplankton grazing,
Europe and North America during the past 50 years,
leading to clear waters and regrowth of aquatic mac
many of which have been successful in improving
rophytes (Gliwicz, 2002). Implicit in this mechanism
water clarity and/or lowering phytoplankton biomass
is a shift in zooplankton from small- to large-bodied
(Drenner & Hambright, 1999). The success of bio
species (e.g., Daphnia) which reduce phytoplankton
manipulation has been variable (Mehner et al., 2002),
biomass and increase clarity, due to higher grazing ef
thus
ficiency (Brooks & Dodson, 1965; Shapiro & Wright,
studies elaborating the
mechanisms
through
which fish removals alter ecosystem function are of in
1984; Carpenter et al., 1985). However, benthivorous
fish (e.g., carp in North America) can structure aquatic
216
systems through many processes and it is uncertain
greater depths (Barko & Smart, 1981; Skubinna et al.,
which processes are prominent in the switch of spe
1995) and sustain significant biomass in the absence
cific ecosystems to higher water clarity following fish
of foraging benthivores that uproot vegetation (Criv-
removal (Mehner et al., 2002).
elli, 1983). Reestablishment of macrophytes following
Several mechanisms may lead to changes in lentic
fish removal can provide positive feedbacks, which
ecology after fish removal from shallow ecosystems,
help stabilize the clear-water phase. Macrophytes may
including direct mechanical effects, direct and indir
maintain high water clarity by competing with algae
ect effects on the nutrient supply, and alterations to
for nutrients and light (Van Donk et al., 1993; Per-
food-web structure. For example, water clarity may
row et al., 1997), providing refugia for zooplankton
increase following benthic fish removal simply due to
(Timms & Moss,
a reduction in suspended sediment. Benthivores feed
creasing sedimentation of suspended particles (James
on invertebrates inhabiting the sediment by sucking in
& Barko, 1990), and suppressing algal growth (Wium-
sediment, catching the invertebrates in their gill rakers
Anderson et al., 1982).
1984; Schriver et al.,
1995), in
and resuspending sediment (Scheffer, 1998). Benthi-
The cause of increased water clarity following fish
vorous fish can have substantial effects on turbidity
removal is commonly attributed to trophic cascading
due to sediment bioturbation (Meijer et al.,
1990;
Breukelaar et al., 1994; Lougheed et al., 1998).
(McQueen, 1990) but conclusions may be confoun
ded by changes in bioturbation and nutrient cycling
Another mechanism that may increase water clar
after fish removal (McQueen, 1990; Vanni & Find-
ity following fish removal is a reduction in phyto-
lay, 1990; McQueen et al.,
plankton biomass through a decreased supply of phos
this study was therefore to examine the multiple im
1992). The purpose of
phorus (Boers et al., 1991). Because benthivores can
pacts of benthivorous fish removals in the temperate,
increase phosphorus concentrations through the recyc
eutrophic Ventura Marsh. Ventura Marsh is a large,
ling of nutrients from the sediment as well as by direct
shallow, windy system located in a predominately ag
nutrient excretion (Lamarra, 1975; Brabrand et al.,
ricultural watershed. Prior to manipulation, the marsh
1990; Vanni & Findlay, 1990; Havens, 1991; Breuk
had a large population of carp which are known to
elaar et al., 1994), benthivore removal can result in
increase phosphorus concentrations (Lamarra, 1975;
direct reductions in ambient phosphorus concentra
Brabrand et al., 1990; Vanni & Findlay, 1990; Havens,
tions (Meijer et al.,
1989; Van Donk et al.,
1990;
1991; Breukelaar et al., 1994), increase phytoplank
Hanson & Butler, 1994; Meijer & Hosper, 1997; cf.,
ton biomass (Tatrai et al., 1997), increase turbidity
Bonneau, 1999; Lougheed, 2000).
(Scheffer, 1998), and reduce submerged macrophytes
Although shifts from small- to large-bodied zo-
(Barko & Smart, 1981; Crivelli, 1983; Roberts et al.,
oplankters following fish removal can result from
1995; Skubinna et al., 1995). This paper describes
reduced preferential predation pressure on large zo-
the effectiveness of benthivorous fish removal in in
oplankton (Lammens & Hoogenboezem, 1991; Dren-
creasing water clarity of Ventura Marsh and examines
ner & Hambright,
aspects of water chemistry and community structure to
1999), there may be other ex
planations. Because grazing by large zooplankton is
elucidate the pathway through which biomanipulation
hindered by suspended sediments (Hart, 1988; Kirk,
functions.
1991), removal of benthivores may reduce turbidity,
allowing larger zooplankton to dominate (Lougheed
& Chow-Fraser,
1998;
Bonneau,
1999).
Even in
Methods
the absence of trophic cascading, decreased suspen
ded sediment following removal of benthivores may
Ventura Marsh is a shallow (mean depth 0.79 m), 76 ha
shift the zooplankton community toward larger-bodied
marsh located in Iowa, U.S.A. (Fig. 1). The marsh is
zooplankton,
fed by surface drainage that forms three concentrated
reducing the phytoplankton biomass,
leading to increased water clarity.
Expansion of macrophyte beds following fish re
inflows from the west, southwest, and south, with an
outlet through a spillway to Clear Lake on the east
moval may further stabilize clear water conditions
ern end. The water level in the marsh is regulated by
(Meijer et al., 1990; Ozimek et al., 1990; Hanson &
the Iowa Department of Natural Resources (IDNR) by
Butler, 1994; Meijer & Hosper, 1997). This may occur
placing boards to the desired level across the outfall.
because the higher water clarity following benthi
This structure was installed approximately 50 years
vore removal can allow macrophytes to expand to
ago to reduce the movement of fish between Clear
217
Clear Lake. Iowa, USA
Farm land
Urban & residential
Grass & pasture
■=> Wetland
133 Forest
Figure 1. Map of Clear Lake watershed showing land use and the location of Ventura Marsh and the reference system. Land-use was determined
using records from the United States Natural Resources Conservation Service, aerial photography and field surveys. Straight, dark lines are
roads and the outside boundary on the map indicates the limit of the watershed determined by GIS from digital elevation maps.
Lake and Ventura Marsh, but the fish barrier system
has fallen into disrepair. Prior to treatment, the fish
fauna of Ventura Marsh was primarily black bullhead
Table I. Ecosystem and water quality conditions for Ventura Marsh
and reference system (Little Clear Lake). Values are averages
of data collected during the pre-manipulation period (12 April
1999-16 August 1999)
(Ictalurus melas) and common carp (Cyprinus carVentura Marsh
pio), which have colonized the marsh since the failure
The western bay of Clear Lake (Little Clear Lake),
to which Ventura Marsh is a tributary, was monitored
Mean depth (m)
Area (ha)
as a reference site for this study (Fig. 1). The Little
Secchi transparency (in)
Lake is a suitable reference site because it is sim
Total phosphorus (|tg 1~' as P)
Total nitrogen (mg 1~' as N)
Silica (mgl"1 asSiO2)
NH++NH3(ngr' asN)
Total suspended solids (mg I"')
ilar to Ventura Marsh in nutrient regime, size, and
depth (Table 1), and is exposed to the same seasonal
variability.
The IDNR conducted the fish removals via applic
Reference
system
of the fish barrier.
0.79
76
0.26
391
5.45
1.13
127
0.32
228
4.70
81
62
1485
1262
86
68
ation of rotenone. To gauge the success of the rotenone
treatments, gill net surveys were performed in con
junction with the IDNR. Three gill nets, measuring
48.8 m long with 6.4 cm bar mesh, were placed for
24 hours in Ventura Marsh on four occasions (3 Au
gust 1999, 10 September 1999, 12 April 2000 and
and the lengths of the first 50 fish of each species were
measured.
We began studying Ventura Marsh in the spring of
21 June 2000). The fish captured were identified and
1999 and the fish removal was planned to occur at
counted. During the last three gill net surveys, carp
the end of the summer of 1999. The IDNR applied
were counted by size category (< 1.8 kg or > 1.8 kg).
rotenone aerially to Ventura Marsh on 17 August 1999
There was reason to believe that the carp population
at the rate of 4 ppm (Fish Kill 1 = FK1). Gill net
was becoming re-established in late summer of 2000,
surveys following FK1 indicated a carp reduction of
so electroshocking was conducted on 1 September
2000. Two transects were shocked for 7 min each. The
fish captured during electroshocking were identified
less than 50%. Perrow et al. (1997) suggests a con
servative target of 75% fish reduction, so a second
attempt to reduce the fish population was conducted in
218
7
be
2
11
be
10
abc
12
c
1
abc
13
be
9
B
c
_2 Kilometers
Figure 2. Map ot Ventura Marsh showing the water quality, plankton, and benthic sampling sites. Points where plankton, benthic samples, and
water samples are indicated by lower case letters.
the winter of 1999/2000. The water level of the marsh
We assessed water quality variables at three sites
was lowered to 51.8 cm below crest and rotenone was
in Ventura Marsh (Fig. 2) and at the deepest point in
applied under the ice on 13 February 2000 to induce
the Little Lake. Dissolved oxygen, temperature, pH,
a winterkill (FK2). Following the second rotenone ap
and conductivity were measured at each half-meter in
plication, approximately 50% of the carp population
terval in the water column. We also collected water
had been eradicated. A third attempt to reduce the fish
samples for analysis of total nitrogen, nitrate, ammo
population occurred in the spring of 2000 (FK3). The
nia, total phosphorus, silica, and total, inorganic, and
water among the cattails surrounding the marsh may
volatile (by combustion at 550 °C for 1 hour) suspen
have provided a refuge for fish during FK1. To re
ded solids at these depths. Total nitrogen and nitrate
duce this possibility, the water level of the marsh was
were analyzed using the second derivative method
lowered to 61 cm below crest in June 2000, reducing
(Crumpton et al., 1992). The remaining analyses were
the amount of water in the cattail beds. Rotenone was
conducted according to standard methods (American
aerially applied at the rate of 8 ppm on 7 June 2000.
Public Health Association, 1998). Secchi disk read
A gill net survey indicated that the fish population
ings were also taken at these three sites.
had been reduced by at least 75% following the third
rotenone application. We could not reliably estimate
Plankton and benthos samples were collected in
excess to make sure that sufficient sampling preci
the size distribution of fish after FK3 since we were
sion was obtained. In August of 1999 we expanded
only able to catch a few fish in nets after these three
our sampling of plankton and benthos from three
rotenone treatments.
replicate samples to 13 replicate plankton samples
To determine the mechanism(s) by which benthi-
and seven replicate benthic samples (Fig. 2). Fewer
vorous fish removal influenced Ventura Marsh, we
benthic samples were taken because we felt that the
studied water quality, plankton, benthos, and macro-
distribution of benthos was more homogeneous than
phytes before and after this series of fish kills (i.e.,
that of the plankton community. We counted a num
FK1-FK3). Water quality, plankton, and benthic com
ber of randomly chosen samples from each date that
munities were sampled every 2 weeks from April
was sufficient to yield an inter-replicate standard er
through October of 1999 and every 2 weeks from
ror of <20% of the mean (Downing, 1979). After
March through September of 2000, with a higher fre
counting many of the 1999 plankton samples, it was
quency of sampling employed following summer fish
noticed that four phytoplankton and three zooplankton
removals. Water quality and phytoplankton samples
samples were sufficient for most dates. We therefore
were collected from the reference system (Little Clear
reduced the number of samples collected in 2000 to
Lake) every two weeks on the same days as we
six phytoplankton and five zooplankton samples. We
sampled Ventura Marsh.
219
continued to collect seven replicate benthic samples
were identified to genus and Copepoda to subor
on each date in 2000.
der using the keys of Pennak (1989). We estimated
The phytoplankton samples were comprised of
zooplankton dry biomass by applying length-weight
equal volumes of water taken from each half-meter
equations (Dumont et al., 1975; Rosen, 1981) with
interval and were preserved with Lugol's solution
the exception of Keratella spp. The biomasses of Ker-
(American Public Health Association, 1998). Samples
atella spp. were estimated from biovolume (Ruttner-
were concentrated and sub-sampled with a Hensen-
Kolisko, 1977) assuming a specific gravity of 1.0 and
Stempel pipette.
a wet to dry weight ratio of 0.05 (Schindler & Noven,
The volume of each sub-sample
varied between 2-5 ml depending on cell density. Us
ing an inverted microscope, we identified, counted,
1971).
The grazing rate potential of cladocerans and ro
and measured phytoplankton. Samples were counted
tifers were approximated using abundance data and
until the most abundant species reached 125 except
estimated clearance rates from the literature (Haney,
when Oscillatoria was most abundant. OsciUatoria
1973;
was often present in very high densities, so when
Lacroix, 1990; Grosselain et al., 1996). The analyses
Bogdan &
Gilbert,
1982;
Mourelatos &
Oscillatoria was most abundant, samples were coun
of Peters & Downing (1984) were not used because
ted until Oscillatoria counts reached 1000. Fifty cells
those authors note the potential impact of container
of each taxon were measured for each sample, ex
effects and other laboratory artifacts on predictions
cept Oscillatoria, for which 250 cells were measured.
from their models. Copepods were not included in the
Phytoplankton were identified to genus, with the ex
estimation of grazing rates because only harpacticoid
ception of small Cyanobacteria, using the keys of
and cyclopoid copepods were present in this study,
Ward & Whipple (1959) and Whitford & Schumacher
neither of which are substantial suspension feeders
(1984). Phytoplankton cells were measured and wet
(Pennak, 1989).
biomass estimated by applying basic geometric formu
The sediment of Ventura Marsh is organic mud so
lae (Findenegg, 1974). From this information, we cal
we were able to obtain benthic samples with an Ekman
culated the biomass of edible (<30 |im) and inedible
grab and filled a one liter bottle with this sediment. We
(>30 \im) phytoplankton (Watson et al., 1992).
filtered the sediment samples through a 600-fxm sieve,
We used a 30-1 Schindler-Patalas trap with a 61-
and the portion remaining in the sieve was preserved in
|xm mesh net to collect zooplankton samples from
5% Formalin solution with sucrose and 100 mg I"1 of
the onset of the study until 23 May 2000, at which
rose bengal (Mason & Yevich, 1967). We counted and
time we began sampling using a 61-jJim mesh Wis
identified all benthic organisms in the samples using
consin net. We switched to a Wisconsin net because
the keys of Pennak (1989) and Merritt & Cummins
we were unable to submerge the Schindler-Patalas
(1996). The first 25 chironomids and 30 oligochaetes
trap without disturbing the sediment during periods
in each sample were measured. Dry masses of Diptera
of low water in 2000. To determine the difference in
and Gastropoda were estimated using length-weight
efficiency between these two sampling devices, both
equations (Eckblad, 1970; Benke et al., 1999). We
collection methods were used simultaneously on three
estimated oligochaete dry mass based on biovolume
sampling dates. In terms of biomass, the Schindler-
(Smit et al., 1993). The standing density of benthos
Patalas trap was found to be approximately 5% more
was estimated on a per unit volume basis to simu
efficient than the Wisconsin net. Therefore, zooplank
late availability to benthivorous fish. Densities were
ton biomass values from Wisconsin net samples were
therefore determined by dividing total dry mass by the
corrected such that they express the expected biomass,
volume of the collection bottle.
had the Schindler-Patalas trap been used. Zooplank
In order to evaluate the impact offish manipulation
ton samples were preserved in 5% Formalin solution
on submerged macrophytes, we conducted macro-
with sucrose (Haney & Hall, 1973) for a minimum of
phyte surveys in July 1999 and August 2000. Twelve
two weeks and were later transferred to 70% ethanol.
north-south transects were evenly spread throughout
Samples were sub-sampled using a Hensen-Stempel
the open water and surveyed in 1999. We recorded
pipette to obtain a volume with a minimum of 60 or
the species present along these transects. In 2000,
ganisms (McCauley, 1984). We identified, counted,
the open water of the marsh was surveyed for sub
and measured zooplankton using a stereomicroscope
merged macrophytes with 27 north-south transects
with 50 x magnification. Twenty-five individuals of
located 50 m apart. A one-meter square quadrat was
each taxon were measured. Rotifera and Cladocera
placed approximately every 20 m along these tran-
220
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==
a>
0.06
0.04 —
Q.
CO
ZJ
CO
g
id
'c
0.02 —
CO
£>
o
c
—
o.oo
i
July
0.2
i
r
August
September
2000
Figure 3. Inorganic suspended solids and Secchi disk transparency for Ventura Marsh during the clear water phase (7 June 2000-27 September
2000), alter the third fish removal (FK3).
sects. We identified the species in the quadrats and
1 September 2000 (a few months after FK3), two tran
visually estimated the percent cover of each species.
sects in the marsh were electroshocked. A total of 73
Direct
comparisons
of
water
quality
values
fishes (68 common carp, 4 buffalo, and 1 bullhead)
between the four time periods (pre-manipulation, post-
were captured in transect one. Only seven fishes (6
FKl, post-FK2, and post-FK3) could be confounded
common carp and 1 buffalo) were captured in transect
by seasonal variability. To reduce this likelihood, the
2. The carp were primarily small fish with an average
before-after-control-impact (BACI) method of ana
length of 15.7 cm and a range of 11.9-26.7 cm.
lysis (Smith et al.,
1993) was used to determine
whether differences in nutrient concentrations, sus
Secchi disk transparency was generally quite low
in the marsh (~0.35 m) but was significantly higher
pended solids, Secchi disk transparency, and phyto-
following FK3 (BACI, p < 0.05). The highest Secchi
plankton biomass were statistically significant among
disk transparency of 1.0 m was recorded on 13 July
the four time periods. Little Clear Lake was used as
2000 (Fig. 3), 6 weeks after FK3. The Secchi disk
the reference system in these analyses.
transparencies from 10 May 2000 to 19 July 2000 were
slightly underestimated since the Secchi disk reached
the marsh bottom at one or more of the sites without
Results
Prior
to
disappearing from view. The period following FK3 is
rotenone
applications,
gill
nets
placed
overnight in Ventura Marsh collected 170 common
carp (Cyprimis carpio) (Table 2). After FK1 and FK2,
113 and 84 common carp were collected respectively.
Of the carp captured following FK1, 54% were very
large fish (>1.8 kg), while only 11% of the carp cap
tured following FK2 were large. Despite lengthy gill
net sets, only 2 common carp, both less than 1.8 kg in
weight were collected following FK3 in June of 2000,
indicating that the majority of the carp population had
been eradicated by the three rotenone applications.
Thirty-one bullheads (Ictalurus melas) were collected
after FK1, but none were captured on the other collec
tion dates. The gill net surveys conducted may not be
an accurate indicator of the bullhead population since
the nets had a large mesh size (6.4 cm bar mesh). On
therefore referred to the 'clear-water phase' and all
prior periods as the 'turbid phase'.
Total phosphorus concentrations were somewhat
reduced in the period following FK3 compared to the
pre-manipulation and the post-FKl periods (BACI,
/; < 0.058). In the pre-manipulation and the post-FKl
periods, the total phosphorus of Ventura Marsh was,
on average, 147 and 216 |ig I"1, respectively, higher
than the total phosphorus concentration of the refer
ence system, whereas in the clear-water phase, the
average difference was only 32 \ig I"1. By inference,
therefore, carp removal resulted in a 115-184 [ig I"1
reduction in total phosphorus concentration in the
marsh.
In the turbid phase, total phosphorus and
phytoplankton biomass were strongly correlated (r2 =
0.73; p
< 0.001) but were not strongly correlated
221
200
400
600
BOO
Total Phosphorus (/yg M)
Figure 4. The relationship between total phosphorus and phyloplankton biomass (A) during the 'turbid' phase (12 April 1999-6 June 2000)
and (B) during the 'clear water' phase (7 June 2000-27 September 2000). Phytoplankton biomass and total phosphorus were strongly positively
correlated during the turbid phase (r2 = 0.73; p < 0.001), but were not signUicantly correlated in the clear water phase (r2 = 0.23; p > 0.05).
during the clear-water phase (r2 = 0.23; p > 0.05)
silica showed no significant changes in concentrations
(Fig. 4).
among the four treatment periods (BACI, p > 0.05).
Ammonia concentrations following FK3 were sig
Inorganic suspended solids (ISS) concentrations in
nificantly different from the pre-manipulation and the
the water column did not differ significantly among the
first post-manipulation period (BACI, p
0.05).
four treatment periods (BACI, p < 0.05), although the
On average, the ammonia concentrations of Ventura
lowest concentration of ISS occurred during the clear-
<
Marsh were 198 and 234 [xg I"1 higher than the ref
water phase (Fig. 3). Linear regression of ISS and
erence system during the pre-manipulation and the
Secchi disk depth in the clear-water and turbid phases
post-FKl periods, respectively. Following FK3, am
showed an overall negative correlation (r2 = 0.51;
monia concentrations in the marsh were, on average,
/; < 0.001) (Fig. 5), however.
387 fig I"1 lower than the reference system. By infer
ence therefore, carp removal resulted in a >600 |xg 1~'
nificantly lower than during the other three treat
reduction in ammonia. Total nitrogen, nitrate, and
ment periods (BACI, p
Volatile suspended solids following FK3 were sig
<
0.05). During the pre-
manipulation and the post-FKl periods, volatile sus-
222
1.2 —
1.0 —
o
spare
ranj
•
Turbid Phase
o
Clear Waler Phase
D
_
O
0.8 —
0.6 —
\-
_
Uish
i
0.4 —
0.2 —
i
1
0.00
0.02
i
i
i
0.04
.
0.06
0.08
Inorganic Suspended Solids (g M)
Figure 5. Relationship between Secchi disk transparency and inorganic suspended solids (/-2 = 0.51; p < 0.001). Solid circles indicate data
from the turbid phase (12 April 1999-6 June 2000) and open circles indicate data from the clear water phase (7 June 2000-27 September 2000).
Table 2. Fish captured during gill net surveys on Ventura Marsh using three 48.8 m long nets with 6.4 cm bar mesh.
Gill nets were placed for 24 hours in Ventura Marsh on four occasions: 3 August 1999, 10 September 1999, 12 April
2000, and 21 June 2000. The fish captured were identified and counted. Common carp (Cyprinus carpio), black
bullhead (lctaluras melas), and channel catfish {Ictalums punciatus) were captured. Common carp were categorized
as either < 1.8 kg or > 1.8 kg. Asterisk (*) indicates that the captured carp were not categorized. The large mesh size
may account for the absence of bullheads on three of the four sampling dates
Date
Common carp
Carp
Bullhead
Channel catfish
size class
Pre-manipulation
Post-FKl
3 August 1999
10 September 1999
170
*
113
61 (> 1.8 kg)
0
2
31
1
0
0
0
0
52 (< 1.8 kg)
Post-FK2
12 April 2000
84
9(> 1.8 kg)
75 (< 1.8 kg)
Post-FK3
21 June 2000
2
0(> 1.8 kg)
2 (< 1.8 kg)
pended solids of Ventura Marsh were, on average,
chi disk transparency showed a strong negative linear
2 and 7 mg I"1 greater than the reference system,
relationship with phytoplankton biomass across the
respectively. Volatile suspended solids during the post-
FK2 period were, on average, 2 mg I"1 less than the
turbid and clear phases (r2 = 0.55,0.74; p < 0.001).
Phytoplankton biomass steadily increased through
reference system, while during the post-FK3 period,
out 1999 and a similar trend began in 2000 (Fig. 6).
volatile suspended solids were 22 mg I"1 lower than
After FK3, however, the phytoplankton biomass de
the reference system. Volatile suspended solids in
creased from 23 mg I"1 to 2 mg I"1. Total phyto
clude both phytoplankton and organic detritus, and
plankton biomass and cyanobacteri a biomass appeared
were thus reduced by nearly 30 mg I"1. No signific
to be slightly higher in 1999 than in 2000. Oscillat-
ant difference in phytoplankton biomass was detected
oria, Actinastrum, and small cyanobacteria were more
among the four periods (BACI, p = 0.05). However, a
prominent in 1999, while Closterium, Merismopedia,
> 20-fold decrease in phytoplankton biomass occurred
and Synedra were predominant in 2000.
between 23 May 2000 and 27 June 2000 (Fig. 6). Sec
ED
D
Dinophyceae
Chrysophyceae
Bacillariophyceae
Chlorophyceae
i\Cyanobacteria
2000
223
in early June and an increase in biomass of Chydorus
pre-manipulation period. There was a peak of Bosmina
at which time the biomass of Daphnia, Ceriodaphnia,
nus. Brachionus began to decrease in late June 2000,
zooplankter to increase following FK3 was Brachio
zooplankton biomass composition (Fig. 7). The first
Following FK3, there were substantial changes to
the rest of the post-FK2 period.
nia were present, but remained very low throughout
Temporal trends in phytoplankton biomass and percent composition of the phytoplankton community in Ventura Marsh from 13 May
1999-27 September 2000. Arrows indicate dates of rotenone applications.
Changes were observed in the zooplankton com
munity across the fish manipulations (Fig. 7). The
during August that remained high until FKL Biomass
zooplankton biomass composition changed during the
of cyclopoid copepods and Keratella was constant
Approximately one month later, the biomass of Bos
cyclopoid copepods, and nauplii began to increase.
mina increased. In early August, Daplmia and Ceriod
during this period. Zooplankton biomass was low fol
toxicity (Beal & Anderson, 1993). There was a small
lowing FK1, which may be attributed to the rotenone
and September of 2000, the zooplankton community
aphnia populations began to decline. By mid-August
consisted mainly of Brachionus, Bosmina, cyclopoid
peak of the rotifer Brachionus, followed by a steady
and nauplii during the post-FKl period. Chydorus
biomass of Keratella, Chydorus, cyclopoid copepods,
copepods, and nauplii.
throughout the post-FK2 period. The zooplankton bio
cladocerans was between 0.2-0.3 mm, whereas, in
cladoceran taxa (Fig. 8). In 1999, the length of most
during this study reflect changes in the prominent
Changes in the size distribution of cladocerans
was very abundant during this period. The biomass
mass in the post-FK2 period was primarily cyclopoid
composition of zooplankton remained fairly similar
copepods. In the spring, cyclopoid nauplii and Daph-
224
■
H
□
U
O
O)
1 I ]
Si
Q Copepod Nauplii
Q Cyclopoidea
1lA
2 —
D
■
2
c
2
IS
Q.
O
O
Ceriodaphnia
Daphnia
Bosmina
Chydorus
Harpacticoida
1 —
Brachionus
Keratellat
N
I
I
I
I
I
I
I
I
I
I
f
Figure 7. Temporal trends in zooplankton biomass and percent composition of the zooplankton community in Ventura Marsh from 12 April
1999-27 September 2000. Arrows indicate dates of rotenone applications. Data are as dry mass.
2000, a larger range of cladoceran lengths was ob
Oligochaetes
and
non-predaceous chironomids
served (0.14-2.06 mm). In 1999, Chydorus was the
were the primary benthic organisms in Ventura Marsh
primary cladoceran while larger cladocerans, such as
(Fig. 10). The composition of the benthic community
Daphnia and Ceriodaphnia, were more prominent in
remained similar throughout the study but the biomass
2000. The distribution of copepod lengths remained
changed considerably. In the pre-manipulation and the
fairly constant throughout the study with a median
post-FK 1 periods, the average biomass of benthos was
length of approximately 0.6 mm (Fig. 8).
22 and 32 mg I"1 of sediment respectively, whereas
Although the estimated grazing rates of cladocer
ans and rotifers peaked a few times before FK3 (i.e.,
in the post-FK2 and FK3 periods, the average biomass
was 95 and 116 mg I"1 of sediment. The length dis
September 1999, June 2000), by far the highest peak
tribution of oligochaetes remained similar throughout
grazing rate potential occurred in July 2000 (Fig. 9),
the study while the median length of chironomids in
some weeks after the fish removal. The July 2000
creased in the post-FK3 period (Fig. 11). The increase
peak in grazing was very high; with nearly 140% of
in size of chironomids in 2000 is likely associated
the marsh water likely filtered each day. During the
with reduced predation from benthivores and not a
turbid phase, grazing rate and phytoplankton biomass
were positively correlated (r2 = 0.42; p < 0.001).
After FK3, however, phytoplankton biomass declined
seasonal trend since an increase in abundance of larger
chironomids was not observed in 1999.
Throughout this study, cattails (Typha) surroun
precipitiously as the abundance of grazers with high
ded the shoreline of Ventura Marsh and clumps of
grazing rates increased (Fig. 9).
Lemna were present throughout the open water. In
225
PreManipulation
FigureS. Box-whisker plot of cladoceran and copepod lengths during pre-manipulalion (12 April 1999-16 August 1999), post-manipulation 1
(17 August 1999-15 October 1999), post-manipulation 2 (14 March 2000-6 June 2000), and post-manipulation 3 (7 June 2000-27 September
2000) periods. Copepod nauplii were not included in these plots. The box represents the middle 50% of the data and the lines represent the
lower and upper quartile. The open star indicates that the mean cladoceran length during post-manipulation 2 was significantly greater than the
mean length during the other three periods. The closed star indicates that the mean cladoceran length in post-manipulation 3 was significantly
greater than during post-manipulation 1. Mean copepod length during post-manipulation 3 was significantly lower than the pre-manipulation
and post-manipulation 2 periods as indicated by the asterisk.
1999, only six of the twelve transects were found
Discussion
to contain any submerged macrophytes. Three taxa
of submerged and floating leafed macrophytes were
The 2-year study of Ventura Marsh provided the op
observed: sago pondweed {Stuckenia pectinata), coon-
portunity to study the effects of a series of benthi-
tail {Ceratophyllum), and water lily (Nymphaea sp.).
vorous fish removals. FK1 eradicated approximately
Potamogeton pectinatus and Ceratophyllum were the
a third of the fish population. Following FK2, the fish
primary submerged macrophytes with only one occur
population had been reduced to about half of the pre-
rence of Nymphaea. All submerged macrophytes in
manipulation level. A greater than 75% reduction in
1999 were found within 5 m of the shoreline. In the
fish abundance was achieved by FK3 in early summer
2000 survey, macrophytes were present along all 27
of 2000. Little change in water clarity or community
transects with over 80% of transects having submerged
structure could be discerned until fish removal was >
macrophytes extending 60 m from shore. Of the 492
75%. By late summer 2000, however, juvenile fish
quadrats sampled, over a fourth had 35% or more cov
became re-established in Ventura Marsh.
erage from submerged macrophytes (Fig. 12). A total
Benthivorous fish removal appears associated with
of 6 genera of submerged macrophytes were found
a reduction in water column phosphorus concentration
in 2000 {Stuckenia pectinata, Elodea, Ceratophyllum,
that may arise through one or both of two mechanisms.
Vallisneria americana,
Although phosphorus did not decline to mesotrophic
Zannichellia palustris,
and
Sagittaria) with Potamogeton pectinatus and Elodea
levels due to substantial nutrient inputs to this eco
being the most prevalent.
system, phosphorus concentrations were reduced in
226
weeks following FK3 and then remained low during
July and August of 2000, indicating a reduced amount
of sediment in the water column possibly due to de
creased benthic fish foraging. An increase in benthos
biomass during the clear-water phase supports the
thesis that fish foraging was low during the clear-water
phase. The high water clarity following FK3 may be
partially due to lower amounts of suspended sediment
as a consequence of reduced fish foraging. Simil
arly, Meijer et al. (1990) attributed increased water
clarity in Lakes Bleiswijkse Zoom and Noorddiep fol
lowing fish removal partially to decreased suspended
sediment due to reduced bioturbation by fish.
1
0
I^l
40
■
I
80
'
The increased water clarity of Ventura Marsh ap
I
120
160
Calculated Grazing Rate (%/day)
Figure 9. Covariation of grazing rates and phytoplankton biomass
following the third fish removal in Ventura Marsh (FK3). The
third rotenone application came at the beginning of the time period
plotted. Point labels refer to dates samples were taken.
peared to also result from reduced phytoplankton bio
mass in the water column. Secchi disk transparency
showed a strong negative relationship with phyto
plankton biomass throughout both the turbid and clear-
water phases (r2 = 0.55,0.74; p < 0.001), indicating
that water clarity increased as phytoplankton biomass
declined. Phytoplankton biomass showed large fluctu
ations in 1999 but overall steadily increased through
Ventura Marsh during the clear-water phase follow
out the summer (Fig. 6). A similar trend began to
ing FK3 compared to the pre-manipulation and the
develop in 2000 with a ten-fold increase in phyto
post-FKl periods (BACI, p = 0.058). Sediment re-
plankton biomass from March to early June. However,
suspension was low during portions of the clear-water
following FK3 in June, phytoplankton biomass de
phase perhaps leading to reduced nutrient recycling
creased to low levels, similar to those observed in 2000
and thus lower phosphorus concentrations. Similarly,
following ice out, for approximately one month.
Havens (1991) observed lower phosphorus concentra
Although the evidence is circumstantial, the re
tions in experimental ponds where fish were prevented
duction in phytoplankton biomass following the third
access to the sediment versus ponds in which fish had
fish removal appears to be due to zooplankton graz
access to the sediment (Havens, 1991). In addition, the
ing. Shortly after FK3, estimated zooplankton grazing
fish removal may have led to lower total phosphorus
rates peaked at 55% of the marsh water per day fol
concentrations due to reduced fish excretion. In Lake
lowed a month later by another peak of around 140%
Gjersj0en, phosphorus released from the roach pop
of the marsh water per day (Fig. 9). The first peak
ulation has been calculated to be on the same order
was due solely to rotifers since cladocerans had not
of magnitude as external phosphorus loading from the
yet become established. During the second peak in
watershed (Brabrand et al., 1990).
grazing, zooplankton biomass was not notably higher,
A short-term clear-water phase was obtained fol
but approximately half of the zooplankton biomass
lowing FK3, involving elements of trophic cascading
was comprised of Daphnia and Ceriodaphnia, which
and changes in physical disturbance. One factor in
were rarely observed on other occasions (Fig. 7). Of
volved in the immediate increase in water clarity in
the cladocerans and rotifers identified in this study,
Ventura Marsh was suspended sediment. This is indic
Daphnia and Ceriodaphnia were the genera with the
ated by the immediate decline in ISS following FK3
highest clearance rates. Phytoplankton biomass re
(Fig. 3) as well as by the strong negative correlation
mained low during these peaks in grazing, suggesting
between ISS and Secchi disk transparency (r2 = 0.51;
that the control of phytoplankton was by zooplankton
p < 0.001) (Fig. 5). Patterns in ISS and Secchi disk
grazing.
transparency tend to mirror one another (Fig. 3). Over
Fish manipulation in Ventura Marsh switched the
all, ISS concentrations were not significantly lower
factor limiting phytoplankton biomass from nutrients
during the clear-water phase (BACI, p = 0.05), how
to zooplankton grazing. The phytoplankton biomass
ever, ISS concentrations steadily decreased for three
seemed to vary with the phosphorus concentration dur-
227
Hirudinea
Ceratopogonidae
Chaoboridae
Gastropoda
Olichochaeta
Chrionomidae
1999
2000
F/^'H/f 70. Temporal trends in benthic hiomass and percent composition for Ventura Marsh from 12 April 1999-27 September 2000. Arrows
indicate dates of rotenone applications.
ing the turbid phase (Fig. 4). Following FK3, however,
(Fig. 1; Arbuckle & Downing, 2001). Overall, phyto
Daphnia and Ceriodaphnia became abundant and the
plankton in Ventura Marsh were correlated with phos
phytoplankton was limited by zooplankton grazing
phorus concentrations until FK3 appeared to switch
(Fig. 9). Zooplankton grazing rates quickly decreased
them to top-down control by herbivorous zooplankton.
from the high peak of 140% in July 2000 to less
Two months later, the system had apparently reverted
than 25% per day. After the decline in grazing in late
back to bottom-up control.
July 2000, phytoplankton biomass began to increase
The maintenance of top-down control is essential
again. Grazing rates remained low (<35% per day)
to a successful fish biomanipulation. It is therefore
during August and September while phytoplankton
important to discern the factors limiting the abundance
continued to grow until limited by nutrient availabil
of large-bodied filter feeding cladocerans. Top-down
ity. The trends in standing phytoplankton biomass in
control occurred following FK3 for approximately two
August and September were similar to the trends in
months when there was a substantial biomass of Daph
total phosphorus, suggesting that the phytoplankton
nia and Ceriodaphnia. Although we were not able
was once again related to phosphorus concentrations.
to collect data on fish diets before manipulation, the
Phosphorus limitation of phytoplankton growth is not
reduction in fish predation by small carp, and lower
uncommon in high nutrient lakes in this region be
suspended sediment in the clear-water phase prob
cause N:P is often quite high due to large amounts
ably accounts for the increase in biomass of these
of fertilizer nitrogen in these agricultural watersheds
larger-bodied cladocerans. The biomass of Daphnia
228
I
Figure
Pre-
Post-
Post-
Post-
Manipulation
FK1
FK2
FK3
11. Box-whisker plot of chironomid and
oligochaete
lengths during pre-manipulation
(12
April
1999-16 August
1999).
post-manipulation I (17 August 1999-15 October 1999). post-manipulation 2 (14 March 2000-6 June 2000). and post-manipulation 3 (7
June 2000-27 September 2000). The box represents the middle 50% of the data and the lines represent the lower and upper quartile. The
star indicates that mean chironomid length during that period (post-manipulation 3) was significantly greater than the mean chironomid length
during pre-manipualtion and post-manipulation 1.
90% coverage
80% coverage
70% coverage
60% coverage
50% coverage
40% coverage
30% coverage
20% coverage
10% coverage
200m
400m
600m
0% coverage
Figure 12. Map of Ventura Marsh showing the percent coverage of submerged macrophytes during the summer of 2000. Map was constructed
based on data from (he August 2000 macrophyte survey. The inverse distance to a power gridding method was used.
229
and Ceriodaphnia began to decline in late July and
macrophytes (Scheffer et al., 1993). The expansion
remained low for the remainder of the study. The
of submerged macrophytes in Ventura Marsh suggests
decline in biomass of larger-bodied cladocerans did
that the higher water clarity may persist in subsequent
not correspond to changes in dissolved oxygen or
years if fish removal could be sustained. Benthivorous
temperature. An increase in juvenile carp and suspen
fish biomanipulations may alter aquatic ecosystems
ded sediment, perhaps due to wind, likely inhibited
through multiple pathways involving trophic cascad
the dominance of larger-bodied cladocerans in late
ing and changes in physical disturbance.
summer.
Even over the short post-manipulation clear-water
phase, the increase in water clarity was sufficient to
Acknowledgements
promote a dramatic increase in macrophyte diversity
and abundance. The higher water clarity and reduced
We are grateful to N. Eckles and B. Cordes for their
uprooting of vegetation may have allowed macro
help in field sampling and lab work. D. Knoll created
phytes to become established at greater depths and at
maps of Clear Lake and Ventura Marsh. We also grate
higher densities. The presence of macrophytes is also
fully acknowledge the Iowa Department of Natural
helpful to the maintenance of high water clarity be
Resources, especially Don Bonneau, Jim Wahl and the
cause they help sustain lower suspended sediment and
crew at the Clear Lake Fish Hatchery, for their sup
lower phytoplankton biomass (James & Barko, 1990;
port assistance and use of equipment. We also thank
Van Donk et al., 1993; Perrow et al., 1997).
two anonymous reviewers who offered constructive
criticisms on the first edition of this manuscript.
Conclusions
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