Download The Impact of Zooplankton Grazing on Phytoplankton

J. Great Lakes Res. 25(1):61–77
Internat. Assoc. Great Lakes Res., 1999
The Impact of Zooplankton Grazing on Phytoplankton Species
Composition and Biomass in Lake Champlain (USA-Canada)
Suzanne N. Levine1,*, Mark A. Borchardt2, Moshe Braner1, and Angela d. Shambaugh1
1School
of Natural Resources
Aiken Center
University of Vermont
Burlington, Vermont 05405
2Marshfield
Medical Research Foundation
Marshfield, Wisconsin 54449
ABSTRACT. Rates of grazing on phytoplankton by macrozooplankton (cladocerans and copepods
> 220 µm in length) and microzooplankton (animals < 220 µm, mostly rotifers and nauplii) were determined for Lake Champlain on three occasions using a modified version of the Lehman-Sandgren method.
Gradients in grazer density were created in fertilized cubitainers incubated in situ, and clearance rates
on specific phytoplankton taxa determined from regressions of algal growth rates on herbivore biomass.
Grazers consumed 3 to 26% of the total phytobiomass present and 22 to 139% of net primary productivity
daily. Macrozooplankton fed most heavily on algae 5 to 25 µm in size and generally selected dinoflagellates and green algae (6 to 26% of biomass removed per day) over cryptophytes (1 to 8%/day), diatoms
(0 to 10%/day) and blue green algae (0 to 6%/day). However, variability in grazing vulnerability among
the species within divisions was high. Microzooplankton had greater weight-specific clearance rates than
macrozooplankton when consuming diatoms, blue-green algae, and cryptophytes, but were less efficient
at harvesting green algae. An experiment in which nutrients and zooplankton were manipulated in a 2 × 3
factorial design indicated that both variables have a net positive impact on phytoplankton growth rates in
Lake Champlain, the zooplankton because they excrete required nutrients. Indirect effects of the nutrients
vs. grazers experiment included rotifer growth in response to increased algal productivity and harvesting
of rotifers and Cladocera by cyclopoid copepods. It was concluded that both nutrients and grazing influenced the structure of Lake Champlain’s phytoplankton community, but that nutrients were generally
more important.
INDEX WORDS: Lake Champlain, zooplankton, phytoplankton, grazing, nutrients, primary productivity, mortality, edibility.
INTRODUCTION
terest in biomanipulation as a tool for reducing
algal biomass when P reductions are difficult
(Reynolds 1994).
The potential for grazing to influence algal biomass has long been recognized. The “clear-water
phase” that is a feature of many lakes in early summer has been attributed to grazing rates that outpace reproduction, the latter being constrained by
nutrient depletion (Sommer et al. 1986). That grazing may account for significant mortality over
longer periods of time is apparent in recent re-evaluations of the chlorophyll a- phosphorus relationship in lakes (Hansson 1992, Persson et al. 1992,
Mazumder 1994). These show chlorophyll a concentrations increasing about four times more
Successful manipulation of forage fish communities through addition or removal of piscivorous fish
and of zooplankton communities through change in
planktivorous fish densities (Reynolds 1994) has
fueled the development of trophic cascade theory
(Carpenter et al. 1985), and raised questions about
the relative roles of nutrients and grazers in controlling algal biomass and species composition in
lakes. While eutrophication management continues
to focus on phosphorus control, there is growing in-
*Corresponding
author. E-mail: [email protected]
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Levine et al.
rapidly with rising total P concentration in lakes
with impoverished zooplankton communities than
in lakes with dense populations of large daphnids.
Biomanipulation experiments have been highly successful in reducing algal biomass when one of their
outcomes has been increased densities of Daphnia
(Liebold 1989, Reynolds 1994). By contrast, manipulations yielding zooplankton communities
dominated by copepods or small-bodied cladocerans rarely have affected phytoplankton.
When zooplankton manipulations affect phytobiomass, phytoplankton species composition is
often altered as well (Porter 1973, Berquist and
Carpenter 1986, Proulx et al. 1996, Svensson and
Stenson 1991). Discrepancies in the relative proportions of phytoplankton species found in the guts of
zooplankton with the proportions present in lake
communities suggest that zooplankton frequently
feed selectively (Porter 1973, Infante 1978,
Berquist and Carpenter 1986), with prey discrimination on the basis of size, shape, toxicity, or nutrient content (Reynolds 1984).
Given the complexity of the pelagic foodweb and
the many factors that affect phytoplankton growth
and mortality, progress in understanding phytoplankton community structure and succession, and
an enhanced ability to predict the outcome of biomanipulation or nutrient management, may require
the use of numeric models. Modeling of phytoplankton dynamics requires quantitative data on reproductive and mortality rates, however, and these
are rarely obtained at the species level. While zooplankton grazing on the total phytoplankton standing stock has been quantified in a large number of
lakes, there is only one substantial data set on the
mortality of individual phytoplankton species during zooplankton grazing, that of Elser and colleagues for three California lakes (Tahoe, Castle,
and Clear; Elser and Goldman 1991, Elser 1992,
Elser and Frees 1995). The intense labor investment
needed to track individual phytoplankton species
has discouraged species-level analysis, as has slow
methods development.
The most reliable method for grazing assessment
is that of Lehman and Sandgren (1985), in which
clearance rates on individual phytoplankton taxa are
estimated by manipulating grazer densities in experimental systems to multiple levels, measuring the resulting growth rates, and regressing algal growth
rates on grazer density. The slope of the regression
line is the clearance rate. However, the approach
provides meaningful rates only if phytoplankton reproduction is “constant” across experimental sys-
tems. Because zooplankton are major recyclers of N
and P (Lehman 1980), and these nutrients frequently
limit phytoplankton growth rate, manipulation of
zooplankton density almost certainly alters reproduction rates under ambient nutrient conditions. To
eliminate the effects of zooplankton nutrient regeneration, nutrients may be added to experimental systems. These saturate nutrient uptake and raise
phytoplankton growth rate to a maximum (and uniform) velocity (Elser 1992). Lehman and Sandgren’s
original method did not include nutrient additions,
so that its use was restricted to consideration of the
general direction (positive, negative, neutral) of net
taxon response to grazer density (Lehman and Sandgren 1985, Berquist and Carpenter 1986). Elser and
Goldman (1991) and Elser (1992) used experimental
systems with and without zooplankton present and
with nutrient saturation to obtain the first estimates
of species-specific grazing mortality in lakes. Cyr
and Pace (1992) and Cyr (1998) then combined the
nutrient additions of Elser with the Lehman-Sandgren method to estimate zooplankton grazing on
total phytobiomass (chlorophyll a) in 16 northeastern U.S. lakes, and grazing on Cryptomonas in two
lakes.
In this work the Lehman-Sandgren technique is
used with nutrient addition to assess taxon specific
phytoplankton loss rates in Lake Champlain. Both
macrozooplankton (animals > 220 µm in length;
Cladocera and copepodite and adult copepods) and
microzooplankton (< 220 µm; mostly rotifers and
nauplii) grazing were assessed on three occasions
(spring, summer, and fall), and compared with phytoplankton division rates (or primary productivity).
A 2 × 3 factorial experiment was also conducted to
compare the importance of nutrients (N + P + C)
and grazers as controls on phytoplankton biomass
in the lake. Lake Champlain is just the fourth lake
worldwide, and the first lake outside of California,
for which rates of macrozooplankton grazing on
specific taxa have been obtained. It is the second
lake for which microzooplankton grazing has been
assessed (the first was Castle Lake, CA; Elser and
Frees 1995). As Lake Champlain shares many
physicochemical and biological characteristics with
the Laurentian Great Lakes, the data presented here
may contribute to an understanding of the phytoplankton dynamics in these important lakes as well
as in Lake Champlain. This work was conducted in
concert with studies of bacterivory and zooplankton-protozoan interactions in Lake Champlain, and
was part of a larger effort to describe and model the
lake’s food web (Levine et al. 1998, 1999).
Zooplankton Grazing of Phytoplankton in Lake Champlain
SITE DESCRIPTION
Lake Champlain is a large (170 km long, surface
area 1,130 km 2 ), deep (maximum depth 122 m;
mean depth 23 m), but narrow (maximum width, 20
km) lake straddling the border between Vermont
and New York and extending a short distance into
Quebec. Numerous islands, sills, peninsulas, and
causeways divide the lake into partially isolated
sub-basins. This study took place in the largest of
these, known as the “Main Lake” (at 44°27′ N,
73°17′ W, about 1 km northwest of Juniper Island,
at the broadest expanse of the lake).
The Main Lake is marginally dimictic; it stratifies in summer, establishing an epilimnion with a
depth of 10 to 12 m, and, in winter, sometimes
freezes for as long as 2 months (February to April).
For several months between October and June,
however, it mixes to the bottom. The Main Lake is
oligotrophic-mesotrophic, with a mean total phosphorus concentration of 0.4 µM (VT Dept. Environ.
Consev., unpub. data) and a mean chlorophyll a
concentration of 5 µg/L (NY Dept. Environ. Consev., unpub. data). Its phytoplankton community is
dominated by diatoms and cryptophytes during
much of the year, although blue-green algal dominance is common in late summer (McIntosh et al.
1993). Seasonal phytoplankton biomass distribution
is bimodal, with a major peak in spring and a
smaller peak in fall. The zooplankton community is
a mixture of cycloploid copepods, cladocerans
(principally Daphnia galeata mendota and Daphnia
retrocurva), and rotifers (McIntosh et al. 1993).
Calanoid copepods are comparatively scarce. In a
typical year, copepods and rotifers are most abundant in spring, while cladocerans peak in summer.
Over 80 species of fish are present in Lake Champlain; Osmerus mordax dentex (rainbow smelt) is
the dominant planktivore (Myer and Gruendling
1979).
METHODS
Grazing Experiments
The Lehman-Sandgren method with nutrient addition was used to estimate zooplankton grazing
rates. Three levels of grazer density were created in
duplicate in transparent 10-L cubitainers for both
macrozooplankton (animals retained by a 220 µm
mesh; adult and copepodite copepods, and cladocerans) and microzooplankton (< 220 µm; rotifers
and nauplii) and the cubitainers incubated in situ
for 2 to 3 days. Phytoplankton growth rates in cu-
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bitainers were obtained by measuring phytoplankton biomass four or more times during an incubation, and calculating the slope of the regression of
ln (phytobiomass) against time. These rates then
were regressed against grazer biomass to yield estimates of grazer-biomass specific clearance rates
(from the slope). The fraction of phytoplankton biomass removed per day was calculated as the product of clearance rate and ambient zooplankton
biomass and carbon flow from the product of this
value and the C content of the phytoplankton (about
0.5 µg C/ µg dwt; Reynolds 1984).
Grazing losses were estimated for several abundant species, for the phytoplankton divisions, and
for the phytoplankton community as a whole. Separate estimates for micro- and macrozooplankton
grazing were possible because the slope of the relationship between algal growth rate and grazer biomass was not affected by an across-the-board
subtraction of grazer biomass from all data points
(provided that the biomass subtracted is of the same
type, which it was). The sieve used to manipulate
macrozooplankton densities allowed microzooplankton to pass freely and thus attain similar densities in all macrozooplankton treatments, while the
microzooplankton treatments used water pre-sieved
to remove macrozooplankton (some contamination
occurred; see below). The experiment was repeated
three times, in mid-summer (25 to 27 July) and fall
(27 to 29 September) 1994, and in spring (8 to 11
May) 1995.
Water and plankton for the experiment were obtained with a clear vertically-oriented 8-L van Dorn
bottle which was deployed at 1-m intervals over the
depth of the epilimnion (10 m in summer, 18 m in
fall) and 2 m into the metalimnion. In spring, when
the lake mixed to the bottom, water collection
stopped at 20 m. The collected water was pooled in
a 240-L tank, and mixed with a paddle, prior to dispersal to cubitainers or sieving. Zooplankton for the
“high macrograzer” treatment were obtained with a
202 µm-mesh Wisconsin net (collar off; mouth diameter 0.5 m; a mason jar attached) towed vertically over the same depth interval used for water
collection. The captured animals were added to 30
L of lake water (under the water surface to minimize air trapping under cladoceran carapaces) to
create a macrozooplankton “concentrate.”
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Levine et al.
The procedure for preparing the experimental
treatments was as follows. The “ambient macrograzer” (AMA) cubitainers received unaltered lake
water from the reservoir, while the “high macrograzer” (HMA) treatment was created by filling cubitainers with lake water and adding sufficient
zooplankton concentrate to increase animal densities about 4 fold (300 to 500 mL). The water remaining in the reservoir then was passed through
either a 202 µm plankton net (July) or a 220 µm
sieve (September and May) to remove macrozooplankton. The “low macrograzer” (LMA) treatment
(which also served as the “ambient micrograzer”
(AMI) treatment) consisted of cubitainers filled
with this coarsely-sieved water. To create the remaining treatments, some of the 220 µm (or 202
µm) “sievate” was passed through a second 20 µm
sieve. The finer “sievate,” which had been largely
cleared of micrograzers, was poured into cubitainers to become the “low micrograzer” (LMI) treatment, while animals collected on the sieve
were washed back into 20 L of the 220/202 µm
“sievate” to produce the “high micrograzer” (HMI)
treatment.
Once all the cubitainers were filled, KH 2PO 4,
NH4Cl, and dextrose (C6H12O6) were added to each
to increase P, N, and C concentrations by 3, 5, and
34 µM, respectively. Air was squeezed out of the
cubitainers to prevent animal trapping in an air
space, and the cubitainers were suspended from anchored floating frames in Burlington Harbor at a
depth of 1.5 m. They were incubated 44, 48, and 64
h in summer, fall, and spring, respectively. Light intensities in the cubitainers were generally below the
threshold for photoinhibition for most phytoplankton groups (< 1,000 µmol/m 2 /s), but still sufficiently high during mid-day (> 300 µmol/m2/s) to
saturate photosynthesis.
Sixty-milliliter phytoplankton samples were collected in triplicate from the cubitainers immediately
before incubation, on 3 or 4 occasions during the
first 24 h of incubation, and daily thereafter. One
percent acid Lugol’s solution was used as a phytoplankton preservative. Zooplankton were collected
at the beginning of each experiment by passing 10
L of the water from the mixing tank through either
a 64 µm (July and September 1994) or 20 µm-mesh
sieve (May 1995), and washing the retained animals
into sample bottles. These samples were used to estimate lake standing stocks. To estimate zoobiomass in the cubitainers, the entire contents of each
cubitainer were sieved (same mesh sizes as the initials) at the end of each experiment. The animals
collected on sieves were anesthesized in carbonated
water prior to preservation in 5% buffered sucrose
formalin (Haney and Hall 1973) with rose bengal
stain.
Algal species composition and cell densities were
determined by direct microscopic counts of settled
samples using an Olympus inverted light microscope (150 random fields, or > 300 cells of the
dominant species). The biovolume of each phytoplankton species was estimated from its cell dimensions and geometry. For common species, cell
dimensions were measured during every incubation
and in all treatments; scarce species were measured
during at least one incubation. Algal dry weight
was estimated from biovolume using the conversion
factor 0.47 pg dwt/µm3 (Reynolds 1984).
Zooplankton were enumerated and measured
with the same compound microscope. The entire
sample was counted for macrozooplankton, while
subsamples were used to estimate microzooplankton numbers. Dead and moribund animals and nonfeeding stages (eggs and embryos) were counted
but not included in biomass estimates. The biomass
of rotifers was estimated from shape dimensions
and geometry (Ruttner-Kolisko 1977), and that of
copepods and cladocerans from biomass-length relationships (McCauley 1984, Culver et al. 1985).
To the extent possible, the relationships used were
for animals preserved as in our study. Preservation
can cause shrinkage of animals, although it is generally minimal (5 to 10%) in 4 to 5% sucrose formalin (Dumont et al. 1975, Culver et al. 1985). The
first two copepodite instars of cyclopoid copepods
were included in the estimates of herbivore biomass
as these animals consume substantial amounts of
phytoplankton. Later stages (especially adults,
which contributed > 90% of copepod biomass in the
experiment) are predominantly carnivorous, and
thus were not included.
Primary Productivity
The y-intercepts of the Lehman-Sandgren regression lines provided estimates of algal division rates
in cubitainers (growth in the absence of grazers).
Multiplying these rates by phytoplankton biomass
and C content yielded estimates of net primary productivity (NPP) under the conditions of the experiment (1.5 m incubation depth, and nutrient
enrichment). To assess primary productivity within
the lake, the 14C technique in a laboratory incubator
was used (Fee et al. 1992). Water was collected as
in the grazing experiments on the second day of the
Zooplankton Grazing of Phytoplankton in Lake Champlain
last two grazing studies (in September and May),
and incubated with 14C-labelled bicarbonate at five
light intensities and at ambient temperature. A
LiCor light meter and submersible probe were used
to estimate light extinction rates at the sampling
site, while a second light meter with an aerial probe
monitored solar irradiance over the course of the
grazing experiments. The numerical model of Fee
(1990) was employed to estimate daily primary production from the data on solar irradiance, light extinction, and productivity-light relationships.
Dissolved inorganic carbon was estimated from
sample alkalinity and pH.
The Nutrients vs. Grazers Experiment
To evaluate the relative importance of nutrients
and grazers in determining Lake Champlain’s phytoplankton standing stocks, a 2 × 3 factorial experiment was performed (31 July to 4 August 1995).
Water and zooplankton were collected as in the
grazing experiments (depth interval, 0 to 15 m) and
the same “high,” “ambient,” and “low” macrograzer
treatments were created, except that each treatment
was repeated in six, rather than two, cubitainers.
Half of the cubitainers at each grazer level then
were enriched with C, N, and P (as in the grazing
experiments), while the other half were left unfertilized. Duplicate chlorophyll a samples (750 mL)
were collected at the beginning of the experiment
from the tanks used to fill cubitainers, and from the
cubitainers after 23 and 92 hr of incubation at 1.5 m
depth. Pigments collected on GFF filters (nominal
pore size 0.7 µm) were extracted in hot ethanol
(Sartory and Grobbelaar 1984), and their absorbance read on a Shimadzu UV-VIS 160U spectrophotometer, using the monochromatic procedure
(665 nm) with phaeophytin correction (Lorenzen
1967). Phytoplankton growth rates were calculated
from the rate of change in chlorophyll a concentration over the incubation. Triplicate phytoplankton
samples (for microscope counts) also were taken
from cubitainers at the beginning and end of the 4day experiment and those in the fertilized systems
were used to obtain a fourth set of grazing and NPP
rate estimates. Zooplankton were collected at the
experiment’s end using the procedures described
earlier. Two-way analysis of variance (ANOVA) allowed assessment of the relative contributions of
nutrients and zooplankton in controlling phytoplankton growth rates.
65
RESULTS
Grazing Studies
Experimental Conditions
The three grazing studies were conducted at the
beginning, middle, and end of the growth season to
maximize the number of phytoplankton species examined and to provide a sense of grazing rate variance. Physicochemical and biological conditions
were markedly different during the three experiments (Table 1). In May, the lake was isothermal,
with a water temperature of 5°C, and nutrient concentrations relatively high. The lake was fully stratified in July, with a mixed layer depth of 10 m and
an epilmnion temperature of 22°C, whereas in September, thermocline erosion was underway (epilimnion temperature, 17°C; mixed-layer depth, 18
m). Phytoplankton biomass was far greater in May
than during the other experiments (Fig. 1) and
strongly dominated by diatoms (96%), in particular
Aulacoseira sp. (67%). The July phytoplankton
community was dominated by green algae
(Mougeotia sp., Oocystis spp., and Eudorina elegans) and cryptophytes (Chroomonas sp. and Cryptomonas sp.), and the September community, by
diatoms and cryptophytes, although blue-green and
green algae were also common.
During two of the three grazing experiments,
Cladocera (Daphnia galeata mendotae, Daphnia
retrocurva, and Eubosmina coregoni) were the principal herbivores present (Fig. 2). The calanoid copepods Diaptomus sicilis and Diaptomus minutus
shared dominance with Cladocera during the May
experiment, but otherwise were scarce. The rotifer
community was consistently dominated by Keratella
spp, but Polyarthra spp., Noltholca sp. (May 1995),
and Kellicottia longispina were present as well. The
predaceous rotifer Asplanchna sp. was common in
July and large enough to be included in the macrozooplankton. Cyclopoid copepods were the most significant components of the carnivorous zooplankton
community. These animals were almost as abundant
as Cladocera in May (dominants Diacyclops
thomasi, Acanthocyclops robustus, and Tropocyclops
prasinus prasinus), scarce in July, and the major contributors to zoobiomass in September (A. robustus,
Mesocyclops edax, and D. thomasi).
Extent of Zooplankton and Phytoplankton
Manipulation Through Sieving and Addbacks
Through sievings and additions of netted animals, 6 to 60 fold gradients in herbivore biomass
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Levine et al.
TABLE 1. Conditions at the sampling site during the 4 experiments. The chemistry data are from the
Vermont Department of Environmental Conservation, and pertain to samples taken within a week of the
experiments. All values pertain to the mixed layer, and are for daytime.
Physicochemical Parameters
Mixed layer depth (m)
Secchi depth (m)
Temperature (°C)
TP (µM)
TDP (µM)
TN (µM)
DIN (µM)
TN:TP
DIN:TP
DSi (µM)
July 1994
Grazing Studies
Sept. 1994
May 1995
Nutrients vs. Grazers
July 1995
10
5
22
0.32
0.13
29
12
89
36
2.9
18
6.5
17
0.29
0.13
38
10
130
33
25
70
—
5
0.35
0.19
49
—
139
—
—
12
6
22
0.29
0.23
23
—
79
—
8.2
Biological Parameters
Chlorophyll a (µg/L)
1.5
2.1
6.3
1.8
Phytobiomass (µg dwt/L)
146
274
1,264
20
Zooplankton Biomass (µg dwt/L)
79
1,282
695
1,144
Herbivore Biomass (µg dwt/L)1
79
371
485
648
Primary Productivity
in fertilized cubitainers (mg C/m3/d)
15
13
119
5
in the lake, areal (mg/m2/d)2
—
349
1,660
—
Limiting Nutrient3
N+P
N+P
None
1Excludes biomass associated with late-stage cyclopoid copepods.
2Cloudless conditions are assumed for the sake of comparability. The estimates include phytoplankton exudates and
thus are approximately gross primary productivity. The values for the cubitainers are net productivity, without respiration and exudates).
3Results of enrichment experiments conducted within a week of the grazing studies at the same sampling site (Levine et
al. 1997).
were created within the macrograzer portion of our
experiments (0.06 to 3.4, 0.003 to 0.25, and 0.09 to
0.58 mg.dwt zoop./L, in May, July, and September,
respectively). The biomass of micrograzers present
in the macrograzer treatments was both fairly uniform, and a minor portion of total zoobiomass (Fig.
2). Thus the estimates of macrograzing can be considered to be relatively free of a “micrograzer influence.” Duplication of macrozooplankton biomass
within treatments was sometimes poor, but this was
not an issue, as data from each cubitainer were entered separately into the regression analysis.
In the microzooplankton portion of the study, the
greatest herbivore biomass present in cubitainers
exceeded the lowest by 200 to 1500 fold. Some of
the LMI cubitainers were almost devoid of animals
(0.0001 to 0.0005 mg dwt/ L), while zoobiomass in
the HMI cubitainers reached 0.61, 0.019, and 0.24
mg .dwt/ L in May, July, and September, respectively. Sieving of lake water through a 220 µm sieve
or a 202 µm net prior to micrograzer manipulation
succeeded in removing > 95% of macrozooplankton
biomass. However, it was not uncommon for one or
two macrograzers to slip through or around the
sieve. Because these animals had biomasses three
orders of magnitude greater than those of the individual microzooplankton, and microzooplankton
were relatively scarce, the estimates of total herbivore biomass in the micrograzer treatments were affected by macrozooplankton contamination;
macrograzers made up from 13 to 57% of the biomass in the AMI treatments, and 36 to 44% of that
in the HMI treatments. In estimating microzooplankton clearance rates, the influence of macrozooplankton grazing was accounted for as follows:
macrozooplankton clearance rates for the taxa of in-
Zooplankton Grazing of Phytoplankton in Lake Champlain
FIG. 1. The biomass of different phytoplankton
groups in cubitainers at the beginning (I) and
ending (F) of incubations with macrozooplankton
at three different densities (low (LMA), ambient
(AMA), and high (HMA). The two sets of columns
indicate duplicate treatments. Incubation times
were 44, 48, and 64 h in July, October, and May,
respectively.
terest (from the macrozooplankton experiment)
were multiplied by the biomass of macrograzers in
cubitainers to yield estimates of the fraction of phytobiomass removed per day. These were added to
the measured growth rates, yielding estimates of
growth rates in the absence of macrograzer contamination. Finally, the corrected growth rates were regressed on micrograzer biomass to obtain the
clearance rates reported.
Phytoplankton communities were not altered by
macrozooplankton sievings and addbacks during
the July and September experiments (Fig. 1). In
67
FIG. 2. The biomass of major zooplankton
groups in experimental cubitainers at the end of
the three grazing studies. HMA, AMA, and LMA
refer to high, ambient, and low macrograzer densities; HMI, AMI, and LMI, to high, ambient, and
low micrograzer densities. The two sets of columns
indicate duplicate treatments. The “lake” samples
were taken at the initiation of the experiments
from the 240 L tank used to fill cubitainers. Lack
of rotifers and nauplii in the “lake” in July is due
to these two samples accidentally being concentrated with a 90 µm rather than a 64 or 20 µm
sieve prior to counting; the sieve probably allowed
rotifers to pass.
May, however, colonial diatoms (Aulacoseira sp.,
Tabellaria spp., and Fragilaria crotonensis) dominated the phytoplankton. These colonies were sufficiently large to be partially retained by the
zooplankton net and added to the HMA treatment
along with zooplankton. Thus the HMA treatment
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Levine et al.
FIG. 3. The biomass of different phytoplankton
groups in cubitainers at the beginning (I) and
ending (F) of incubations with microzooplankton
at three different densities (low (LMI), ambient
(AMI), and high (HMI). The two sets of columns
indicate duplicate treatments. Three levels of
microzooplankton density were used. Incubation
times were 44, 48, and 64 h in July, October, and
May, respectively.
had a phytoplankton biomass 2 to 3 times greater
than the AMA and LMA treatments. Manipulation
of micrograzers with a 20 µm sieve did not influence cryptophyte abundance in cubitainers, but did
affect the densities of larger algae, especially those
forming colonies (Fig. 3). The HMI cubitainers
therefore contained about three times as much phytobiomass, and the LMI cubitainers only one half as
much, as was present in the lake (AMI). The expected effects of these manipulations on grazing
rate estimates are considered below.
Primary Productivity
The y-intercepts of the Lehman-Sandgren curves
provided estimates of phytoplankton division rates
in the cubitainers, albeit under the nutrient- and
light-enhanced conditions of the incubations. These
rates were 0.20, 0.09, and 0.18 /d in July, September, and May, respectively. Multiplying these values
by phytobiomass and C content yielded net primary
production (NPP) estimates of 15, 13, and 119 mg
C/m3/d. These rates can be compared with 14C estimates of gross primary productivity (GPP) at the
incubation depth during September and May, 56
and 184 mg C/m3/d respectively. The latter were
greater, despite the fact that they were for unfertilized conditions, because they include C exuded
from algae or respired during the 2 day incubations
used to estimate NPP.
For the lake as a whole, areal primary production
(GPP) estimates of 236 and 1,093 mg C/m2/d were
obtained in September and May, respectively. These
rates (the first ever reported for Lake Champlain)
reflect partially cloudy weather. Under cloudless
conditions, the areal rates would be 349 and 1,660
mg C/m2/d. The mixed layer was much deeper in
May than in September (70 vs. 18 m), and the phytoplankton, although more abundant, were more
light limited (Levine et al. 1999). The mean volumetric GPP rates for the mixed layer during September and May were 13 and 16 mg C/m 3 /d,
respectively. Under cloudless conditions, they
would be 19 and 24 mg C/m3/d.
Grazing Rates
Rates of phytoplankton loss from Lake Champlain as a result of macrograzing were very low in
July and September 1994, < 1% of total phytobiomass per day, and only modestly higher in May
(10% per day). Losses to microzooplankton were
slightly greater and followed the same seasonal
trends, 4, 3, and 15% per day, in July, September,
and May, respectively. Microzooplankton made up
a relatively small proportion of total zoobiomass,
but had weight-specific clearance rates four or more
times those observed among macrozooplankton
(Tables 2 vs. 3), hence the similarity in grazing
pressure.
Expressed as a percentage of the NPP in cubitainers, macrozooplankton and microzooplankton
removal rates for total phytobiomass were 2, 0, and
56% and 20, 33, and 83% in July, September, and
May, respectively. Thus in May, grazers removed
more phytobiomass per day than was produced,
Zooplankton Grazing of Phytoplankton in Lake Champlain
69
TABLE 2. Clearance rates (CR; mL/day / µg dwt zoopl.) for macrozooplankton feeding on phytoplankton and estimates of percentage algal biomass lost per day during the four studies in Lake Champlain.
Rates are given for the total phytoplankton community, for algal divisions containing > 10% of phytoplankton biomass, and for a selection of individual species. Clearance rates significantly different from
zero at P > 0.05 are indicated with an asterisk. GALD = greatest axial linear dimension.
Taxon
Total
GALD
—
July 1994
C R % Lost
0.06
0.4
Sept. 1994
C R % Lost
–0.02
0
May 1995
C R % Lost
0.26
10
July 1995
C R % Lost
0.17
11
—
0.18*
–0.01
0.15
—
—
—
0.19
—
1.69*
0.41*
0.13*
0.08
0.07
—
By Division:
Greens
Cryptophytes
Diatoms
Blue greens
Dinoflagellates
—
—
—
—
—
By Species:
Mougeotia sp.
Coelastrum scabrum
Cryptomonas sp.
Chroomonas sp.
Aphanizomenon flos-aquae
Chroococcales
Fragilaria crotonensis
Tabellaria sp.
Aulacoseira sp.
Centrales1
1An unidentified, small species,
18
1.8
13
—
—
—
—
—
—
11
—
—
1.8*
58
—
—
—
—
7
1.79
12
0.28
9
—
—
0.46
28
4
–0.59
0
0.06
2
—
—
0.09
6
32
—
—
–0.05
0
—
—
—
—
2
—
—
—
—
0.14
9
27
—
—
0.00
0
—
—
—
—
17
—
—
–0.01
0
—
—
—
—
13
—
—
—
—
0.16
8
—
—
2
–5.63
0
—
—
—
—
0.05
3
not colonial. This estimate does not include grazing on other Centrales, like Aulacoseira.
0.92
0.12
–0.68
–0.39
2.11
6
1
0
0
15
—
7
0
6
—
—
—
10
—
89
26
8
5
4
—
TABLE 3. Clearance rates (CR; mL/day / µg dwt zoopl.) for microzooplankton feeding on phytoplankton
and estimates of percentage phytobiomass lost per day, during the three grazing studies in Lake Champlain. Rates are given for the total phytoplankton community and for algal divisions containing > 10% of
phytoplankton biomass. Clearance rates significantly different from zero at P > 0.05 are indicated with an
asterisk.
Taxon
Total
CR
2.28
By division:
Greens
Cryptophytes
Diatoms
Blue-greens
0.81
4.40
—
—
July 1994
% Lost
4
1
7
—
—
contributing to the collapse of the spring bloom.
For the September and May experiments, grazing
can also be expressed as a percentage of the mean
GPP rate in the 18 and 70 m-deep mixed layers; the
values are 22 and 658%.
Sept. 1994
CR
% Lost
*
1.07
3
May 1995
CR
% Lost
*
0.83
15
—
2.15*
0.33
2.64*
—
—
1.12*
—
—
6
1
7
—
—
20
—
Discrepancies in taxon vulnerability to macrograzers were apparent both at the Division level and
among species within a Division (Table 2). During
July, dinoflagellates lost 15% of their standing
stock to grazing daily, while green algae lost 6%,
70
Levine et al.
and cryptophytes, 1%. Blue-green algae had negative clearance rates (grew more rapidly in the presence of grazers), and thus probably were largely
invulnerable to grazing. In September, when dinoflagellates and green algae were scarce, cryptophytes and blue-green algae were subject to greater
grazing mortality, 7 and 6% per day, respectively.
Diatoms also were present at this time, but apparently not utilized by grazers (loss rate, 0% per day).
In May, diatoms, the biomass dominant, lost an average of 10% of their biomass per day to macrograzers, which in this case included copepods as
well as Cladocera. Micrograzers consumed cryptophytes, blue-green algae, and diatoms at higher
rates than did macrograzers (Tables 2 vs. 3). During
the spring bloom, they removed 20% of diatom biomass daily. Micrograzers were somewhat less efficient than macrograzers at green algal consumption,
perhaps because the green algae present were relatively large.
Table 2 includes rates of macrozooplankton grazing on some of the more abundant phytoplankton
species. Grazing by microzooplankton at the
species-level was not measured because of the low
densities of the species involved. Among the cryptophytes, Cryptomonas sp. was more vulnerable to
macrozooplankton predation (11 to 12% loss per
day) than Chroomonas sp. (loss rate, 0 to 2% per
day). Among the blue-green algae, the Chroococcales were more heavily grazed than Aphanizomenon flos-aquae, and, among diatoms,
Aulacoseira sp. suffered greater grazing losses than
Fragilaria crotonensis and Tabellaria sp.
Many of the clearance rates given in Tables 2 and
3 are not significantly different from zero at a P
level of 0.05. This is partly because clearance rates
were, in fact, very low, but also because of scatter
related to the patchy distribution of large (especially colonial) and rare phytoplankton species and
the strong influence of individual animal length on
zoobiomass estimates (all animals were assumed to
have a mean length, when length actually varied).
Although the regressions would have been greatly
improved by the omission of outliers, this was
avoided, given that there was no knowledge of what
the correct grazing rates were. The reporting of
large grazing rate estimates not significantly different from zero should be viewed as provisional.
Nutrients Versus Grazers
The nutrients vs. grazers experiment took place
at the same time of year as the July grazing experi-
ment, but a year later. Epilimnion depth, temperature, and nutrient concentrations were nearly identical during the two studies. Phytoplankton species
composition was similar in the 2 years (Figs. 1 vs.
4), but phytobiomass was 7 times lower and herbivore biomass, 8 times greater in 1995. In addition,
cyclopoid copepods (mostly Mesocyclops edax)
were abundant in 1995, but scarce in 1994 (Fig. 2
vs. 5). This was essentially a “clear water” phase.
Samples taken 23 h into the experiment indicated
little change in chlorophyll a concentrations relative to initial values (Fig. 6), suggesting that phytoplankton may need a day or more to “gear up” for
nutrient assimilation and division (Reynolds 1984),
and also that grazing was not particularly intense.
FIG. 4. The biomass of major phytoplankton
groups in experimental cubitainers at the beginning (I) and end (F) of the nutrients vs. grazers
experiment, July 1995. The three sets of columns
indicate triplicate treatments.
FIG. 5. The biomass of major zooplankton
groups in experimental cubitainers at the end of
the nutrients vs. grazers experiment, July 1995.
The three sets of columns indicate triplicate
treatments.
Zooplankton Grazing of Phytoplankton in Lake Champlain
71
FIG. 6. Chlorophyll a concentrations in experimental cubitainers 0, 23 and 92 h into the nutrients vs. grazers experiment, July 1995. Initial concentrations were measured for the water used to
fill cubitainers of similar treatment. The three sets
of columns indicate triplicate treatments.
FIG. 7. Phytoplankton growth rates vs. (a) total
zooplankton biomass and (b) herbivore biomass
(late stage cyclopoids excluded) of July 1995.
Trend lines are linear regressions. The one shown
in Panel b is for fertilized cubitainers.
After 92 h, however, most nutrient-enriched cubitainers had chlorophyll a concentrations substantially above initial values, as did cubitainers with
elevated zooplankton densities. By contrast, those
cubitainers that were left unfertilized and with zooplankton densities at or below ambient levels
showed no increase in chlorophyll a. Two-way
ANOVA indicated that both nutrient and zooplankton levels had a statistically significant (p < 0.05),
and positive, impact on phytoplankton growth rates
during the 3 days of the experiment when chlorophyll a levels increased (23 to 92 h). The nutrientzooplankton interaction term was trivial.
A plot of phytoplankton growth rate in cubitainers versus total zooplankton biomass (herbivores
plus carnivores) revealed only a weak relationship
between the two variables under nutrient enrichment, but a strong positive relationship when no nutrients were added (Fig. 7). Growth rates declined
sharply with herbivore biomass in the fertilized sys-
tems, but, in the unfertilized systems, they first increased and then decreased as herbivore biomass
rose above 0.5 mg/L. The slope of the relationship
between growth rates and herbivore biomass for
fertilized and unfertilized systems was similar
above the 0.5 mg/L threshold, suggesting that in
both treatments, phytoplankton divided at maximal
rates when zooplankton were dense enough to keep
the nutrient supply high. Thus the slopes obtained
reflected grazing impacts alone.
Analysis of zooplankton communities at the end
of the experiment revealed some unexpected treatment side effects. As intended, total zooplankton
and also cyclopoid biomass in cubitainers increased
along the gradient LMA to AMA to HMA, while
nauplii densities were uniform (micrograzers were
not manipulated). Cladoceran biomass, however,
proved to be greater in the AMA than in the HMA
cubitainers, and rotifer biomass peaked at the lowest macrozooplankton level (Fig. 5). Furthermore,
72
Levine et al.
rotifer biomass (mostly Polyarthra and Keratella)
was significantly greater in fertilized than in unfertilized cubitainers. These results suggest that the 4day incubation was too long for maintenance of the
zooplankton community structure imposed by the
treatments. Rotifers, which can reproduce rapidly
due to small size and parthenogenesis, were able to
exploit the greater productivity of the nutrient-enriched systems and increase in numbers, while cyclopoid copepods managed to exert a grazing
impact on rotifer densities. Cyclopoid predation
may have also been responsible for the reduced
cladoceran densities in the HMA treatments.
Macrograzer densities created in fertilized cubitainers permitted an additional set of grazing rate
estimates for mid-summer (Table 2). The findings
were similar to those obtained during the year before: green algae were more heavily grazed than diatoms, cryptophytes, and blue-green algae (26% vs.
4 to 8% of biomass/d), and among the cryptophytes,
Chroomonas sp. was grazed less than Cryptomonas
sp. (6% vs. 28% loss/d). The clearance rate for the
phytoplankton community as a whole was 0.17 mL
per g of zooplankton/d, or 11% of phytobiomass
daily. Using change in chlorophyll a concentration
in the fertilized cubitainers to calculate community
grazing mortality yielded a nearly identical result
(0.18 mL/g zooplankton/d or 11% of biomass/d).
All grazing estimates derived from the nutrients
versus grazers experiment may be slightly below
real values because of the growth of rotifers in the
fertilized LMA treatment. These animals likely
contributed to a lowering of the algal growth rate in
the cubitainers involved, with the result that the
growth rate vs. zoobiomass curve was less steep
than it otherwise would be. Net primary productivity was especially low during this experiment (5 mg
C/m3/d).
DISCUSSION
Macrozooplankton Grazing on Phytoplankton
This study provided much needed data on taxonspecific rates of phytoplankton mortality due to
zooplankton grazing. Modeling of phytoplankton
community dynamics requires such information,
but only one study prior to this has yielded rate estimates for taxonomic levels finer than the entire
community. With this study, the list of analyzed
species is expanded from warm temperate species
to those found in boreal regions and the Great
Lakes.
Like Elser and Goldman (1991) and Elser (1992),
substantial variability in the vulnerability of phytoplankton taxa to macrozooplankton consumption
was found. Some species lost as much as 58% of
their biomass per day to grazers, while others were
unaffected. A few had negative grazing rates, indicating that they grew more quickly when zooplankton were abundant than when they were rare. These
species are likely immune to grazing and benefit
from the suppression of more vulnerable phytoplankton species, either because this suppression releases resources for their use or because the
suppressed species are active in allelochemical
production.
Much of this assessment was done at the Division
level. Most conclusions were in agreement with
previous findings and with widely-accepted concepts about the role that grazers play in influencing
algal community structure; a few were not. Because
Cladocera dominated during all but the May experiment (when calanoid copepods were also important), these observations pertain primarily to this
group of herbivores.
One important paradigm of phytoplankton ecology is the existence of low grazing pressure on
blue-green algae, which presumably are toxic
(Arnold 1971), of low nutrient content (Lampert
1981), or too large and filamentous for easy consumption (Lampert 1981, Infante and Abella 1985).
Blue-green grazing mortality was consistently minimal (< 1% per day) during the experiments.
Another group frequently described as relatively
inedible is the dinoflagellates (Porter 1977, Sommer et al. 1986). However, higher grazing rates
were measured on this group than on any other, and
these results are not unique. Elser (1992) reported
grazing rates on Gymnodinium similar to ours, and
Proulx et al. (1996) described the blooming of dinoflagellates in a Quebec lake following the removal of zooplankton through planktivorous fish
introduction. Dinoflagellate vulnerability may depend on size, and the species seen during the experiments were relatively small (except for Ceratium
hirundinella).
Among the phytoplankton generally considered
most edible are cryptophytes, chrysophytes, and
small non-colonial diatoms (Porter 1977, Sommer
et al. 1986). Chrysophytes were too rare in Lake
Champlain during this study to permit estimation of
their losses to grazers, while the response of cryptophytes to grazing was mixed. Cryptomonas sp. was
as strongly grazed as green algae and dinoflagellates, while Chroomonas sp. suffered minimal
losses. Many other researchers have reported heavy
Zooplankton Grazing of Phytoplankton in Lake Champlain
grazing on Cryptomonas (e.g., Porter 1977, Lehman
and Sandgren 1985, Knisely and Geller 1986). The
Cryptomonas clearance rates measured by Elser and
Goldman (1991) and Cyr and Pace (1992) were
even greater than those reported here. That
Chroomonas sp. is poorly grazed may contribute to
its status as the most abundant phytoplankter in
Lake Champlain (McIntosh et al. 1993).
Minimal grazing was observed on diatoms except
for Aulacoseira sp., which was grazed at a rate of
8% per day in May 1995. Because the diatoms present during this study were primarily colonies large
in at least one dimension, this was expected. Elser
and Goldman (1991) measured similarly low rates
of diatom consumption in California lakes. That diatom losses were greater in May than July and September may be related to the greater densities of
calanoid copepods present. Calanoids are more efficient than Cladocera at consuming large particles
(Peters and Downing 1984).
Green algae are a highly diverse group which apparently contains both edible and inedible species
(Porter 1977, Sommer et al. 1986). This group was
found to be one of the most heavily grazed in Lake
Champlain, although some of the algae used as prey
items (e.g., Mougeotia sp.) have been previously
classified as inedible (Knisely and Geller 1986). In
their study of California lakes, Elser and Goldman
(1991; Elser 1992) measured low grazing rates on
most green algae, but relatively high rates for certain species of Cosmarium, Oocystis, Quadrigula,
and Selenastrum.
There were no obvious clues as to why some
species within phytoplankton divisions were more
vulnerable to grazing than others. In some cases,
size may have been a factor. Three of the poorly
grazed species, Tabellaria sp., Fragilaria crotonensis, and Aphanizomenon flos-aquae, were colonies
too large to fit easily into the gap of most cladoceran carapaces or into the mouths of most copepods (Gliwicz 1977). Two colonial species,
Aulacoseira sp. and Mougeotia sp., were moderately grazed, but these algae form singular filaments that grazers can attack by holding down one
end and pulling (or biting) cells off the other (Vanderploeg and Paffenhöfer 1985).
Very small algae may slip though the filtering
setae of grazers (Gliwitz 1977) and thus be captured
at a lower rate than larger algae. The two smallestsized species that were assessed, Chroomonas sp.
(4 µm) and an unidentified centric diatom (2 µm),
were very poorly grazed. A third small-celled
species, Chroococcus sp., was moderately grazed,
73
but it forms small colonies that increase its effective size. The moderately to heavily grazed species
in the experiments were 5 to 25 µm in their greatest
axial linear dimensions (GALD), or formed
colonies of this size. The literature indicates that
the optimal food size for most zooplankton is 10 to
20 µm GALD (Svensson and Stenson 1991).
Differential species vulnerability to grazers
within phytoplankton divisions presents a challenge
to modelers of phytoplankton dynamics. Modeling
the dynamics of dozens of phytoplankton species is
cumbersome. Therefore, phytoplankton are often
compartmentalized by division rather than by
species (e.g., Lehman et al. 1975, Scavia et al.
1988). These results, and Elser’s, indicate that mean
division loss rates mask important dynamics at the
species level. A more fruitful approach may be the
modeling of a selection of particularly abundant
species.
Microzooplankton Grazing on Phytoplankton
In a recent study of Castle Lake, CA, Elser and
Frees (1995) showed that the traditional emphasis
of grazing studies on macrozooplankton may
greatly underestimate overall grazing mortality.
Phytoplankton removal rates by micrograzers in
this lake (5 to 22% of phytobiomass per day) overlapped or exceeded removal rates by macrograzers
(5 to 12% per day). This study of micrograzing in
Lake Champlain also indicated phytoplankton
losses on par with the losses to macrozooplankton
(3 to 14% vs 1 to 10% of phytobiomass per day).
Micrograzers had significantly higher biomass-specific clearance rates than macrograzers when feeding on most phytoplankton divisions (cryptophytes,
blue-green algae, and diatoms). Only green algae
appeared to be more easily cleared from suspension
by macro- than micrograzers. The green algal
species involved (e.g., Mougeotia sp., Oocystis
spp., and Coelastrum scabrum) were relatively
large or colonial in nature, and thus presumably difficult for a small animal to handle.
Phytoplankton species > 20 µm in size were manipulated substantially by the sievings and addbacks preceding the micrograzer experiment. All
phytoplankton divisions except the Cryptophyta
were affected. Because clearance rates decline with
food density (as the inverse of the cube root; Peters
and Downing 1984) and growth rates rise with diminished mortality, the impact of unequal phytoplankton densities on the Lehman-Sandgren curves
is expected to be a reduction in slope (as the point
74
Levine et al.
at high grazer density rises), and thus an underestimation of grazing rates. Thus microzooplankton
may be even more important grazers than the values
in Table 4 suggest. A recent study by Cyr (1998)
suggested that zooplankton communities dominated
by rotifers or copepod nauplii generally have higher
biomass-specific clearance rates than communities
dominated by Cladocera or adult copepods.
Champlain is that of a slowly-growing phytoplankton community cropped by zooplankton feeding at
a similarly slow pace. Analysis of zooplankton-protozoan-bacterial interactions in the cubitainers indicated that, while phytoplankton were the principal
food source for zooplankton in May, bacteria and
heterotrophic protozoa were more important in July
and September (Levine et al. 1999).
Total Grazing Loss
Micro- and macrozooplankton together removed
from 2 to 21% of the phytoplankton biomass in the
mixed layer of Lake Champlain daily. Cyr and Pace
(1992) reported exactly the same range of removal
rates for 30 phytoplankton communities in 16
northeastern U.S. lakes (they analyzed grazers > 80
µm, and thus included the bulk of micrograzers).
The similarity of the two ranges indicates that temporal variability in grazing rates may be of a similar
order of magnitude to lake-to-lake variability, and
should be considered when phytoplankton grazing
is modeled.
Comparisons of grazing loss rates with phytoplankton replacement rates have more ecological
significance than comparisons with standing stocks.
However, estimates of species-specific reproductive
rates are almost as rare as species-specific grazing
mortality estimates. The estimates of reproductive
rates reported here were for artificial conditions
(more light and nutrients than normally enountered
in the lake), but they are useful in forming first
order approximations of grazing as a fraction of
production. The combined mortality induced by
macro- and microzooplankton grazing balanced
from 22% to 139% of the NPP measured in fertilized cubitainers. Thus, grazing is a more important
phenomenon in Lake Champlain than the slow biomass loss rates suggest. Grazing should be more
significant yet when related to the lower NPP rates
expected in the absence of nutrients. When contrasted with the mean primary productivity of the
lake’s mixed layer (the 14C estimates), grazing mortality was relatively minor in September (22%), but
exceeded primary production by 6 fold in May. Cyr
and Pace (1993) reported that, on average, zooplankton remove 51% of lacustrine primary production annually.
Reproductive rates in the cubitainers were on the
low end of values reported for natural phytoplankton communities in the literature, 0.1 to 0.2 versus
0.1 to 0.9 per day (Reynolds 1984). Thus the image
of phytoplankton dynamics that emerges for Lake
Nutrients Versus Grazers
as Phytoplankton Controls
The nutrients vs. grazers experiment supported
the view that nutrients play a major role in regulating algal biomass in Lake Champlain. Combined
additions of N, P, and C to cubitainers increased
phytoplankton growth rates, even at the highest
grazer level (ANOVA indicated a nutrient level effect at p < 0.03). Other researchers conducting field
experiments of a similar design have noted the
same effect (Lehman and Sandgren 1985, Berquist
and Carpenter 1986, Vanni 1987, Kivi et al. 1993,
Spencer and Ellis 1998). At the division level, response to nutrients was more variable. Diatoms and
green algae generally increased with fertilization,
while cryptophytes and blue-green algae sometimes
were negatively affected, or showed no consistent
response (Fig. 4; also Levine et al. 1997). Lehman
and Sandgren (1985) and Berquist and Carpenter
(1986) also found negative responses to fertilization
among some species in their experiments.
While it is generally expected that grazers should
reduce phytobiomass and thus growth rates,
ANOVA indicated a significant (p = 0.01) positive
relationship between the phytoplankton growth
rates in cubitainers and macrozooplankton level.
Lehman and Sandgren (1985) and Berquist and
Carpenter (1986) also observed phytoplankton
species whose growth rates increased on elevation
of zooplankton levels. Both Kivi et al. (1993) and
Spencer and Ellis (1998) reported a lack of relationship between chlorophyll a concentration and
grazer level in nutrient versus grazer experiments,
although some positive trends were found in
Spencer and Ellis’s study. Kivi et al. (1993) observed a slightly positive relationship between primary productivity and grazer level, while Elser and
MacKay (1989) reported a stronger relationship.
What is implied by the outcome of this experiment
and those of others is that nutrient recycling by zooplankton has a greater impact on phytoplankton dynamics than does grazing mortality. By examining
algal growth in fertilized and unfertilized cubitain-
Zooplankton Grazing of Phytoplankton in Lake Champlain
ers separately, it was confirmed that the positive relationship between growth rates and zooplankton
level was due to algal response in the nutrient-poor
systems. For the fertilized cubitainers, there was a
negative relationship between growth rate and herbivore biomass.
The nutrients vs. grazers experiment was perhaps
most valuable in revealing the tremendous intertwining of feeding and recycling relationships in
the lake, and thus the potential for indirect consequences to resource or trophic level manipulations.
Nutrient additions stimulated algal growth, which
in turn allowed rotifer growth to increase, providing
more food for cyclopoid copepods. This was just
one of the “cascades” observed. The rotifer increase
also drove down protozoan populations, allowing
bacterial densities to rise (Levine et al. 1999).
These results argue strongly for a modeling approach to phytoplankton ecology, as models are
needed to track multiple permeations of effects.
They also suggest that time limits are necessary on
the field incubations used to calculate grazing rates.
Four days is obviously too long. One to 2 days may
be more reasonable, given that rotifer increases
were not observed during grazing studies of this
length. Brief incubations create problems when
grazing rates are low, however. Substantial sample
replication and intensive phytoplankton counting
are necessary to obtain grazing curves with reasonably high r2 values. Chlorophyll a analysis yielded
estimates of total phytoplankton grazing mortality
similar to those obtained for phytobiomass, and
thus this low-labor method may be used when
species-level analyses are not required.
Future Research
Future research on zooplankton grazing in Lake
Champlain should include separate night time and
day time analyses. This study did not take into account the fact that macrozooplankton undertake extensive vertical migrations that cause them to
concentrate at the surface at night and disperse at
depth during the day. The analysis also should be
extended to other lake sub-basins, and to wintertime sampling. Assessment of cyclopoid copepod
feeding dynamics is desirable, as these largely carnivorous species are common in the lake and may
indirectly affect rates of herbivory. They may also
engage in omnivory when animal foods are scarce
(Adrian and Frost 1993), although they are believed
to be inefficient feeders on algae of the small size
common to Lake Champlain (Knoechel and Holtby
75
1986). Had cyclopoids been included in the estimates of herbivore biomass, the values obtained for
biomass-specific clearance rates would have been
reduced by 5 to 98% (estimates of phytoplankton
loss rates would not be greatly affected as their determination involves multiplication of the lower
clearance rates by greater zoobiomass). Improved
assessment of micrograzing is another priority. The
dilution method of Landry and Hassett (1982) may
allow grazers to be manipulated without affecting
phytoplankton. However, when animal and algal
populations are already small, dilution further increases variability in density determinations and
leads to low r2 values for grazer curves (J. Lehman,
Univ. Mich.)
A larger goal is extension of species-specific
grazing analyses to a diversity of lakes around the
world, and comparison of these losses with reproductive rates. Cyr’s (1998) recent comparison of
grazing in lakes with different zooplankton community types indicates that calanoid copepods and rotifers can exert as much grazing mortality on
phytoplankton as Cladocera under oligotrophic conditions. Thus it is particularly important that studies
of species-specific grazing mortality expand beyond the cladoceran-dominated lakes investigated
to date.
ACKNOWLEDGMENTS
We thank H. McKinney for assistance in the field
and laboratory, S. Pomeroy for help with data entry,
and the Vermont and New York Departments of Environmental Conservation for the sharing of unpublished data on nutrients and chlorophyll in Lake
Champlain. J. Lehman, R. Stemberger, A. McIntosh, and an anonymous reviewer provided useful
comments on the manuscript. This project was
funded by the U.S. Environmental Protection
Agency through the New England Interstate Water
Pollution Control Commission (LC-RC92-6NYRFP).
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reproduction by Daphnia pulex fed seven species of
blue-green algae. Limnol. Oceanogr. 16:906–920.
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Submitted: 8 December 1997
Accepted: 18 October 1998
Editorial handling: Marlene S. Evans