Download Seasonal succession in fishless ponds: effects

Hydrobiologia 490: 125–134, 2003.
© 2003 Kluwer Academic Publishers. Printed in the Netherlands.
125
Seasonal succession in fishless ponds: effects of enrichment and
invertebrate predators on zooplankton community structure
Christopher F. Steiner1,2 & Allison H. Roy3
1 W.
K. Kellogg Biological Station and the Department of Zoology, Michigan State University,
Hickory Corners, MI 49060, U.S.A.
2 Present address: Department of Ecology, Evolution, and Natural Resources, Cook College,
Rutgers University, New Brunswick, NJ 08901, U.S.A.
E-mail: [email protected]
3 Institute of Ecology, University of Georgia, Athens, GA 30602, U.S.A.
E-mail: [email protected]
Received 26 February 2002; in revised form 6 August 2002; accepted 20 November 2002
Key words: competition, Daphnia, enrichment, Notonecta, seasonal succession, size-efficiency hypothesis
Abstract
Size-selective predation by fish is often considered to be a primary driver of seasonal declines in large-bodied
Daphnia populations. However, large Daphnia commonly exhibit midsummer extinctions in ponds lacking planktivorous fish. A number of empirical and theoretical studies suggest that resource competition and its interaction
with nutrient enrichment may determine variable dominance by large Daphnia. Low resource levels may favor
competitive dominance by small-bodied taxa while large Daphnia may be favored under high resource conditions
or following a nutrient/productivity pulse. Nutrient enrichment may also influence the strength of invertebrate
predation on Daphnia by affecting how long vulnerable juveniles are exposed to predation. We investigated these
hypotheses using an in situ mesocosm experiment in a permanent fishless pond that exhibited seasonal losses of
Daphnia pulex. To explore the effects of nutrient enrichment, Daphnia plus a diverse assemblage of small-bodied
zooplankton were exposed to three levels of enrichment (low, medium, and high). To explore the interaction
between nutrient enrichment and invertebrate predation, we crossed the presence/absence of Notonecta undulata
with low and high nutrient manipulations. We found no evidence of competitive reversals or shifts in dominance
among nutrient levels, Daphnia performed poorly regardless of enrichment. This may have been due to shifts
in algal composition to dominance by large filamentous green algae. Notonecta had significant negative effects on
Daphnia alone, but no interaction with nutrient enrichment was detected. These results suggest that Daphnia are not
invariably superior resource competitors compared to small taxa. Though predators can have negative effects, their
presence is not necessary to explain poor Daphnia performance. Rather, abiotic conditions and/or resource-based
effects are probably of greater importance.
Introduction
A commonly observed successional pattern in planktonic communities is a seasonal shift from early season
dominance by large-bodied species of Daphnia to late
season dominance by small-bodied Cladocera (such
as Diaphanosoma and Ceriodaphnia) and copepods
(Sommer et al., 1986; Gliwicz & Pijanowska, 1989).
To date, this seasonal dynamic has been investigated
primarily in lake communities with an associated emphasis on size-selective predation by fish as a principal
determinant of zooplankton size-structure (e.g. Sommer et al., 1986; Gliwicz & Pijanowska, 1989; Tessier
& Welser, 1991), a view rooted in the size-efficiency
hypothesis (SEH) of Brooks & Dodson (1965). SEH
postulates that large-bodied zooplankton, compared
126
to small-bodied taxa, are superior resource competitors and consequently dominate in the absence of
predators. Size-selective predation by fish can reduce
the abundance of large taxa, permitting dominance
by small-bodied zooplankton. However, in small permanent ponds where fish are absent, zooplankton
communities frequently exhibit early season peaks followed by midsummer losses of large-bodied Daphnia,
despite the absence of the presumed key determinant (e.g. Fig. 1A; see also Hall et al., 1970; Lynch,
1978; Steiner, 2001). Furthermore, seasonal patterns
of Daphnia relative biomass can vary greatly among
these water bodies, with some systems being dominated by Daphnia for the entire growing season, some
showing successional patterns, and some having little
or no Daphnia (Steiner, 2001). The determinants of
this variation are unknown and hint at a biological
complexity not encompassed within the conventional
top-down view.
Despite the appeal of SEH, a sizable body of
evidence suggests that variable dominance by large
Daphnia may be dependent on interspecific competition and its interaction with environmental context,
independent of fish predator presence or absence (see
DeMott, 1989). For example, a number of studies
have emphasized the importance of resource concentration and system productivity on differential performance of large versus small-bodied Cladocera (e.g.
Goulden et al., 1978; Tillmann & Lampert, 1984;
Romanovsky & Feniova, 1985; Tessier & Goulden,
1987). Low rates of algal-resource supply can favor small-bodied taxa by exposing starvation-prone
juvenile Daphnia to demographic bottlenecks (Neill,
1975a; Romanovsky & Feniova, 1985). High resource
availability (or a pulse of food) can allow Daphnia
populations to accrue a large number of adult stage individuals. These adults could in turn depress resource
levels (via high filtration rates) and essentially outstarve small-bodied competitors. This novel mechanism could explain variation in competitive outcomes
among ponds as well as seasonally within systems,
especially if ponds are prone to mixing events. To
date, a number of studies have suggested that competitive outcomes between large and small zooplankton
could be dependent on initial algal resource levels
or productivity/nutrient pulses during community development (Tillmann & Lampert, 1984; Romanovsky
& Feniova, 1985; Bengtsson, 1987). However, these
studies, in addition to the general model (sensu Romanovsky & Feniova, 1987), do not consider dynamic
algal communities whose composition may change
Figure 1. Zooplankton seasonal dynamics in P14 during the 1997
growing season. (A) Major zooplankton groupings, including
Chaoborus, Daphnia pulex, copepods (cyclopoids and calanoids
combined), and small-bodied Cladocera (all taxa combined). (B)
Copepods and small-bodied Cladocera ungrouped and depicted separately (Alona, Ceriodaphnia, Bosmina, Scapholeberis, and rotifers
were rare, at no time comprising greater than 5% of total biomass,
and have been omitted for clarity). Shown is mean biomass (+1)
from two vertical tows. Error bars are not depicted to improve
clarity.
in conjunction with enrichment events and/or grazing pressure (e.g., Vanni, 1987; Kerfoot et al., 1988).
Shifts in algal composition towards dominance by
127
species resistant to Daphnia grazing could weaken
nutrient effects on Daphnia population responses.
Resource effects notwithstanding, top-down effects could also generate mid-summer declines of
Daphnia in fishless ponds. For example, salamanders
(Notophthalmus and Ambystoma) are common in shallow ponds and can feed preferentially on large-bodied
zooplankton (Dodson, 1970; Morin, 1987). However,
zooplankton communities may still exhibit seasonal
declines in large Daphnia populations even when
predaceous salamanders have been excluded (Morin,
1987). Furthermore, in deeper, open water ponds
(e.g., Fig. 1A) where salamanders are largely absent
in the pelagic zone, successional patterns are still
common (Steiner, 2001). Planktivorous invertebrates
are also plentiful in pond systems, yet how effective
these predators are in shifting the size-structure of
zooplankton communities remains equivocal. A number of studies have documented a general preference
by invertebrate predators for small or intermediate
size classes of zooplankton (Lynch, 1979; Pastorak,
1981; Spitze, 1985), though some species (such as the
backswimming bugs, Notonectidae) can feed on larger individuals (Scott & Murdoch, 1983; Murdoch et
al., 1984; Arner et al., 1998). The potential impact of
invertebrate predators on community size structure is
complicated by differential susceptibility of Daphnia
life stages; juveniles are more vulnerable to predation
but adults may attain a relative size refuge (Swift &
Fedorenko, 1975; Vinyard & Menger, 1980; Spitze,
1985). Consequently, seasonal variation in productivity and/or resource quality may enhance top-down
effects by affecting how long juveniles are exposed
to predators and the ability of individuals to reach a
size refuge (Chase, 1999). Just as a pulse of resource
production may affect competitive outcomes, high
levels of resources may weaken invertebrate predator
interactions with Daphnia.
In the present paper we report on an in situ mesocosm experiment in which we explored these hypotheses and processes in a semi-natural pond known
to exhibit a seasonal loss of large-bodied Daphnia
pulex. The experiment was executed during Daphnia’s midsummer decline. To test effects of a nutrient/productivity pulse on patterns of dominance,
we exposed Daphnia plus a diverse assemblage of
small-bodied zooplankton to three levels of nutrient
enrichment. To examine effects of invertebrate predators and their potential interaction with enrichment,
low and high nutrient levels were further crossed
with presence and absence of the invertebrate pred-
ator Notonecta undulata. If resource abundance, independent of predation, mediates Daphnia performance
in the experimental pond, we predict that Daphnia
should dominate zooplankton assemblages only in
nutrient enriched treatments. Alternatively, if the sizeefficiency hypothesis is operating, Daphnia should
dominate in the absence of predators at all nutrient
levels. Finally, if Notonecta are a primary driver of
Daphnia performance, we predict that the presence
of the predator should shift dominance towards smallbodied zooplankton. Nutrient enrichment may weaken
the shift to small-bodied forms by allowing Daphnia
to attain a size refuge from predation.
Study site
The experiment was performed in a single pond (P14)
at the W. K. Kellogg Biological Station, experimental
pond facility (Hickory Corners, Mich., U.S.A.). This
pond is permanent, fishless, and approximately 1.6 m
deep, at its deepest point, with a surface area of
approximately 700 m2 . P14 is unstained and has a
large open water zone free of submerged macrophyte
cover. Hence, light penetration in the water column
is high. Trophic state of the pond is in the mesotrophic range, with mean total phosphorus (±S.E.)
over three years of 15.3 ± 6.1 µg P l−1 . However,
this phosphorus level is low when considering the
natural range encountered in fishless ponds in the region (Steiner, 2001, 2002). Daphnia pulex (hereafter
referred to as Daphnia) is the only Daphnia species found in the pond. Over 5 years of monitoring
(1996–2000), P14’s Daphnia population has undergone seasonal succession, peaking in abundance in
late spring and then being succeeded by a zooplankton
assemblage dominated primarily by Diaphanosoma
brachyurum and copepods (e.g. Fig. 1A, B). The pond
supports an invertebrate predator assemblage, resident
year-round, dominated by the phantom midge larvae
(Chaoborus americanus; for densities see Fig. 1A).
Backswimming bugs (Notonecta) are also present but
attain much lower densities in the experimental ponds
(7–70 individuals per 10 000 l; Steiner, unpublished
data). Dytiscid beetle larvae have also been commonly observed. Pond temperatures (measured at middepth) during the course of the study averaged 23.5 ◦ C
(range: 21–25.5 ◦ C).
128
Materials and methods
The experiment was deployed June 23–July 25, 1997
(32 days), during the natural decline phase of Daphnia in this pond (Daphnia were completely absent
by the end of the experiment; see Fig. 1A). Our experimental system consisted of impermeable 1200-l
polyethylene ‘bag’ enclosures with a 1-m diameter,
open at their tops, sealed at their bottoms to exclude
sediments, and suspended in the water column by
floating frames. Tops of the frames were covered with
fiberglass screening (1.3-mm mesh size) to deter insect invasion. Water was pumped from the pond, at
mid-depth, into the bags through a 150-µm mesh net
to remove the majority of the zooplankton population. A day after enclosures were filled with water
we inoculated bags with an equal biomass concentration of Daphnia pulex and a diverse assemblage
of small-bodied zooplankton. Small zooplankton were
obtained from a neighboring pond (P9) that contained
a population of sunfish (Lepomis gibbosus) and thus
contained no Daphnia and no invertebrate predators
due to planktivory (personal observation). The zooplankton assemblage extracted from this pond included all the major late-season taxa found in P14,
including species of Diaphanosoma, Ceriodaphnia,
Chydorus, Bosmina, Scapholeberis, calanoid and cyclopoid copepods, and several species of rotifers (dominated primarily by Keratella, Lecane, and Trichocerca). We lab reared all Daphnia pulex to ensure their
availability at the time of the experiment. Zooplankton biomass concentrations in Daphnia cultures and
P9 were based on length-mass regressions (McCauley,
1984) and determined from samples taken a day prior
to inoculation. Total initial zooplankton biomass in
the enclosures was 24.5 µg l−1 , 42% of the natural
biomass level in P14 at the time of the experiment’s
initiation.
To explore effects of a nutrient pulse on zooplankton dynamics we subjected enclosures to three nutrient
treatments (high, medium and low). To examine effects of invertebrate predators we included treatments
with the predator Notonecta undulata at low and high
nutrient levels. All treatments were replicated three
times for a total of 15 enclosures. Nutrient manipulations consisted of additions of phosphorus (Na2 HPO4 )
and nitrogen (NaNO3 ) with a N:P molar ratio of 57:1,
matched to that of the ambient pond water to minimize changes in algal stoichiometry. High nutrient
treatments received a start concentration of 150 µg P
l−1 , medium treatments received 80 µg P l−1 , and low
nutrient treatments received no additions for a start
concentration of 10.7 µg P l−1 . Nutrients were added
once, 1 day after zooplankton additions. Notonectids
for predator treatments were collected from ponds at
the experimental pond facility using horizontal tows
with a plankton net. Each predator treatment received
7 adult Notonecta – on the high end of densities found
in ponds at the experimental facility but low when
considering the range of variation encountered in fishless ponds (J. Chase, Washington University, pers.
comm.). Because Notonectids are known to feed preferentially on Daphnia (Scott & Murdoch, 1983), we
biased our experiment towards seeing predator effects
on the large zooplankter. Predator additions occurred
4 days following zooplankton inoculations.
Beginning on day 8, zooplankton and phytoplankton were sampled every 8 days using an integrated
tube sampler that extended to the bottom of the enclosure. Zooplankton were immediately preserved in
chilled sucrose formalin and stored for later enumeration. Fifty randomly chosen individuals of each species were also measured to obtain dry mass estimates
using length-mass regressions (McCauley, 1984). Water samples (500 ml total) were collected, placed
on ice, and later filtered for subsequent analysis of
chlorophyll a as a measure of algal biomass (sensu
Welschmeyer, 1994). We fractionated samples into
two size classes. Half of the water sample was directly
filtered onto Gelman A/E glass fiber filters to measure
total chlorophyll a. The other half was first filtered
through a 35-µm Nitex mesh to measure the ‘edible’
size fraction of algae. Midway through the experiment
a mat of filamentous green algae (dominated by Oedogonium and Spyrogyra) appeared on the water surface
of the medium and high nutrient enclosures. Surface
algae was collected in totality on the final day of the
experiment using d-nets, subsampled and filtered to
measure chlorophyll a. In all subsequent analyses, we
treat surface algae as grazer resistant.
Biomass responses of zooplankton and algae
through time were analyzed using univariate repeated
measures ANOVA (rm-ANOVA). Analyses of single
sample dates were performed using ANOVA. To explore the effects of nutrient enrichment on zooplankton responses, we analyzed low, medium, and high
nutrient enclosures (without Notonecta) as a one-way
design. To examine the effects of predators and their
interaction with nutrient enrichment, we analyzed low
and high nutrient enclosures with and without predators as a separate 2 × 2 factorial design. Chlorophyll
a measures were log10 transformed to conform to
129
assumptions of homogeneity of variances. Due to
zero values, all zooplankton biomass measures were
log10(x + 1) transformed. All proportional data (percent relative biomass) were arc-sine square root transformed. Due to potential violations of the assumption
of circularity, we present Greenhouse–Geiser (G–G)
adjusted probabilities for all repeated measures analyses (von Ende, 1993). Unless otherwise stated all
time × treatment interactions were not significant.
Statistics were performed using Systat Version 8.0.
Results
Algae appeared to respond positively to nutrient enrichment, as indicated by chlorophyll a concentrations
through time (Fig. 2; p = 0.057, F2,6 = 4.795,
between subjects effect, rm-ANOVA). Relative biomass of grazer resistant (>35-µm) algae was calculated as the difference between total and <35-µm
fractions divided by total chlorophyll. Repeated measures analysis of the relative abundance of this size
fraction revealed weak effects of enrichment (Fig. 3;
p = 0.075, F2,6 = 4.118, between subjects effect,
rm-ANOVA). However, these measures do not take
into account filamentous surface algae. Its inclusion
with day 32 chlorophyll a revealed a strong positive
effect of enrichment on total chlorophyll a (Fig. 4A;
p < 0.001, F2,6 = 44.57, one-way ANOVA) and
on the relative abundance of >35-µm algae (Fig. 4B;
p < 0.001, F2,6 = 36.168, one-way ANOVA).
Focusing on zooplankton responses in the absence
of predation, nutrient enrichment had weak positive
effects on Daphnia biomass (Fig. 5, dashed lines; p =
0.090, F2,6 = 3.695, between subjects effects, rmANOVA). Mid-experiment, Daphnia biomass began
to drop in all treatments and by day 32 there were no
significant differences among nutrient levels detected
(p = 0.248, F2,6 = 1.772, one-way ANOVA). No
nutrient × time interactions were detected (p > 0.10).
Enrichment had positive and sustained effects on total
small-bodied zooplankton biomass (Fig. 5, solid lines;
p = 0.009, F2,6 = 11.539, between subjects effect,
rm-ANOVA). The small-bodied zooplankton response
was largely due to the significant positive responses of
Cladocera to enrichment (p = 0.007, F2,6 = 12.994,
between subjects effect, rm-ANOVA). There was no
effect of nutrients on copepod biomass (p > 0.05,
within and between subjects effects, rm-ANOVA).
In the absence of predators, percent relative biomass of the major components of the zooplankton
Figure 2. Algal responses (not including surface filamentous forms)
to low, medium and high nutrient treatments, in the absence of
predators. Shown are means (±S.E.).
Figure 3. Relative biomass of ‘grazer-resistant’ algae (>35-µm
chlorophyll a, not including surface filamentous algae) over the
course of the experiment in low, medium, and high nutrients treatments, in the absence of predators. Means are shown with one-way
standard error bars. Some treatments have been horizontally offset
for clarity.
assemblage varied greatly through time and as a function of enrichment (Fig. 6). Small zooplankton were
dominated primarily by Cladocera (of which Diaphanosoma, Bosmina, and Chydorus were the dom-
130
Figure 5. Responses of small-bodied zooplankton (solid lines;
cladocera, copepods, and rotifers combined) and Daphnia pulex
(dashed lines) in low, medium and high nutrient treatments, in the
absence of Notonectid predators. Shown are means and one-way
standard error bars. Some treatments have been offset horizontally
for clarity.
Figure 4. (A) Total chlorophyll a (including surface filamentous algae) on the final date of the experiment, in the absence of predators.
(B) Relative biomass of ‘grazer-resistant’ algae (>35-µm chlorophyll a plus surface filamentous chlorophyll a) on the final date
of the experiment, in the absence of predators. Means are shown
(±S.E.).
inant components) and copepods. Rotifers, after day
16, comprised less than 5% of total zooplankton biomass. With the exception of day 16 in the high nutrient
treatment, Daphnia did not dominate the zooplankton
community at any time during the experiment, regard-
less of nutrient enrichment (Fig. 6). Enrichment had no
effect on the relative biomass of Daphnia through time
(p = 0.248, between subjects effect, rm-ANOVA;
p = 0.246, within subjects effect, rm-ANOVA). In
contrast, small-bodied zooplankton comprised, on average, greater that 70% of zooplankton biomass in all
non-predator enclosures.
Notonectids had no effect on the biomass of total
small-bodied zooplankton (Fig. 7A) or its major components – small-bodied Cladocera, rotifers, or copepods (p > 0.17 for all within and between subjects
predator and predator × nutrient effects, rm-ANOVA).
Notonectids did have negative effects on Daphnia
pulex (Fig. 7B), independent of nutrient level (p =
0.012, F1,8 = 10.603, between subjects effect, rmANOVA). However, there were no significant nutrient × predator interactions (p > 0.10, within and
between subjects, rm-ANOVA) nor was a predator ×
time interaction detected (p > 0.10, rm-ANOVA).
This suggests that declines in Daphnia abundance
were not a function of predator presence or absence.
Discussion
As a driver of temporal and spatial variation in
zooplankton community size structure, size-selective
predation by fish has a formidable body of supporting
131
Figure 6. Mean relative biomass of the major components of the
zooplankton community in (A) low, (B) medium, and (C) high nutrient treatments, in the absence of predators. Error bars are omitted
for clarity.
evidence (e.g. Hrbacek et al., 1961; Brooks & Dodson, 1965; Gliwicz & Pijanowska, 1989; Mittelbach
et al., 1995). However, the importance of top-down
effects in fishless ponds is uncertain. Our experi-
Figure 7. Effects of the presence/absence of Notonecta undulata at
low and high nutrients on (A) responses of small-bodied zooplankton and (B) Daphnia pulex. Shown are means and one-way standard
error bars. Some treatments have been offset horizontally for clarity.
ment provided evidence that invertebrate predators can
have negative effects on large-bodied Daphnia populations. Notonectids inflicted significant reductions in
Daphnia populations, a result consistent with previous investigations (e.g. Murdoch et al., 1984; Arner
et al., 1998). Thus, this invertebrate predator has the
capacity to play the role that planktivorous fish do in
132
the original formulation of SEH. Nonetheless, while
biomass was depressed in the presence of Notonecta,
Daphnia at no point dominated the zooplankton community and by mid-experiment had begun to decline
in all enclosures, independent of predator presence or
absence. This was true regardless of nutrient level; enrichment had no effect on the magnitude or strength of
predator effects on Daphnia. Hence, the heart of the
size efficiency hypothesis – competitive dominance by
large-bodied zooplankton in the absence of predators
– was not supported by our experiment. While topdown effects are present and at times strong, variation
in Daphnia dominance need not be invariably linked to
the presence/absence of predators, a conclusion consistent with previous studies of fishless ponds (e.g.
Hall et al., 1970; Lynch, 1978, 1979).
As previously outlined, absolute quantity of resources has been linked to variable Daphnia performance, with several papers suggesting that small-bodied
species perform better at low resource levels and
large-bodied species at high resource concentrations
(Goulden et al., 1982; Tillmann & Lampert, 1984;
Romanovsky & Feniova, 1985; Bengtsson, 1987;
Tessier & Goulden, 1987). Using simulations, Romanovsky and Feniova (1985) have shown that resource
pulses may facilitate competitive reversals by diminishing effects of small-bodied species on Daphnia
and strengthening the negative effects of Daphnia on
competitors. Variation in nutrient availability, and consequently algal production, might be especially high
in shallow water bodies such as ponds in which mixing events extend through the entire water column
to nutrient-rich sediments. Thus, this model may account for variation in competition effects among ponds
(along gradients of productivity and/or mixing regime) as well as variation in competitor interaction
strength within ponds (due to mixing events and seasonal changes in productivity). Though we did not
measure the effects of competition directly in our experiment, the small-bodied assemblage was composed
largely of Cladocera, species known to compete with
Daphnia for shared resources (reviewed in DeMott,
1989). Focusing on relative biomass, Daphnia at no
point exhibited clear competitive dominance, comprising a minor fraction of the zooplankton community at
all times during the experiment. This was true despite
a nutrient pulse an order of magnitude greater than
ambient levels. While Daphnia biomass did increase
in response to enrichment, the effect was short-term
and in clear contrast to the more sustained responses
of the small-bodied zooplankton fraction. Further-
more, the lack of dominance does not appear to be
an artifact of experimental duration since Daphnia responses peaked mid-experiment and then declined in
all treatments.
In order for productivity pulses to generate shifts
in competitive outcomes, Daphnia must exhibit a
substantial population increase and dominate the zooplankton community during the early onset of community development. During this early community
growth phase, adult Daphnia, through their high per
capita filtration rates, can drive resources to low levels
and out-starve competitors (Romanovsky & Feniova,
1985). This dynamic response was clearly not attained in the present investigation suggesting that
abiotic conditions or some aspect of resource quality
may have suppressed Daphnia population responses.
Though the majority of algal production was in the edible range early in the experiment (surface filamentous
forms began to appear by day 16), this course level
of resolution can miss important aspects of resource
quality and algal size structure. For example, zooplankton taxa can vary in their preferences for different particle sizes and taxa (e.g. Neill, 1975b; Knisely
& Geller, 1986; Bogdan & Gilbert, 1987). Compared
to large Daphnia species, many small-bodied species are thought to be more efficient in their use of
small algal particles and bacteria (taxa < 2µm; Neill,
1975b; Geller & Muller, 1981; Pace et al., 1983).
Thus, using a single size-based cut-off to quantify ‘edible’ resources ignores potentially important aspects
of algal size and taxonomic composition. More recently, nutritional adequacy (carbon, phosphorus, and
nitrogen content) has been recognized as an important
aspect of resource quality that may differentially favor
zooplankton taxa (Sterner & Hessen, 1994). Daphnia
have unusually high phosphorous demands compared
to most small-bodied Cladocera and copepods, making them especially prone to phosphorus limitation
(Sterner & Hessen, 1994). We did not measure C:N:P
content of algal resources. However, the TN:TP ratio
in our experimental pond prior to the experiment was
57:1 (molar), indicative of strong phosphorus limitation (Healey & Hendzel, 1980). Thus, stoichiometric
conditions of algal resources were likely unfavorable
for Daphnia. Finally, resource effects could have
interacted with pond temperatures. High temperatures (>25 ◦ C) are known to have a disproportionately
strong negative effect on large-bodied zooplankton,
potentially altering competitive outcomes with smallbodied species (reviewed in Moore & Folt, 1993;
though see Achenbach & Lampert, 1997). In the first
133
weeks of the experiment, pond temperatures averaged 25 ◦ C, levels at which small-bodied zooplankton should have been favored in competition with
Daphnia.
Poor Daphnia performance and declines later in
the experiment may have also been due to our use
of a dynamic resource community. Prior investigations that have uncovered effects of resource concentration on competitive outcomes have used static
algal assemblages (e.g. Tillmann & Lampert, 1984;
Romanovsky & Feniova, 1985; Bengtsson, 1987).
Phytoplankton community composition is known to
change in response to both enrichment and grazing
pressure (McCauley & Briand, 1979; Reynolds, 1984;
Vanni, 1987; Kerfoot et al., 1988; McCauley et al.,
1988). In our study, algae increased in response to
enrichment but also exhibited a striking increase in
the grazer-resistant size fraction. By the termination
of the experiment, much of this was in the form
of surface-bound filamentous algae that comprised
close to 60% of algal biomass in the highest nutrient treatments. If primary productivity is channeled
to species of algae inaccessible to Daphnia, the nonequilibrial dynamics envisioned in Romanovsky &
Feniova (1985) may not be approximated. Other studies have shown that allocation of resource production
towards less edible forms can attenuate consumer biomass responses to enhanced productivity (e.g. Bohannan & Lenski, 1999). Finally, numerous investigations
have shown that filamentous blue-green algae can interfere with feeding of large Daphnia (small-bodied
taxa are less susceptible), potentially altering competitive outcomes with small-bodied Cladocera and
copepods (e.g., Gliwicz & Siedlar, 1980; Sumner &
Dodson, 1983; Gliwicz & Lampert, 1990). In our
study, filamentous forms were composed primarily of
green algae. Though it is not known whether these
species can interfere with Daphnia feeding efficiency,
it is certainly plausible. These results do not negate
the idea that temporally fluctuating resources may facilitate coexistence among competing zooplankton or
that pulses can prolong Daphnia persistence in otherwise unfavorable environments. It does however call
into question the capacity of a nutrient pulse to generate alternative competitive outcomes and Daphnia
dominated systems in natural pond environments.
Our results showed that top-down effects, while
present, are not needed to explain the poor performance of Daphnia following mid-summer declines in
ponds. Rather, abiotic conditions, resource quality,
or competition with small-bodied taxa (or some com-
bination thereof) appear to be more important. The
inability of Daphnia to dominate small-bodied taxa in
the absence of predators is further evidence that SEH
may have limited applicability in shallow pond systems. Finally, the effects of varying resource levels and
productivity on competitive outcomes between large
and small-bodied taxa may be insubstantial outside
of a laboratory setting (i.e. when applied to systems
in which algal composition is dynamic and itself a
function of enrichment and grazing events).
Acknowledgements
We thank Gary Mittelbach, Alan Tessier, Jim Bence,
Don Hall, Steve Hamilton, Jan Bengtsson, and two
anonymous reviewers for comments on earlier drafts
of this manuscript and/or valuable discussions. Several people helped to make these experiments possible;
our thanks go out to N. Dorn, G. Mittelbach, J. Rettig, G. Smith, and J. Wojdak. S. Hamilton aided with
nutrient analyses. This research was supported by a
K.B.S. Lauff Research Award, the M.S.U. Department of Zoology, the K.B.S Research Experience for
Undergraduates program funded by the National Science Foundation, and the K.B.S. Graduate Research
Training Group (RTG) funded by National Science
Foundation grants DIR-09113598 and DBI-9602252.
This is contribution #977 from the W. K. Kellogg
Biological Station, Michigan State University.
References
Arner, M., S. Koivisto, J. Norberg, & N. Kautsky, 1998. Trophic
interactions in rockpool food webs: regulation of zooplankton
and phytoplankton by Notonecta and Daphnia. Freshwat. Biol.
39: 79–90.
Auchenbach, L. & W. Lampert, 1997. Effects of elevated temperatures on threshold food concentrations and possible competitive abilities of differently sized cladoceran species. Oikos 79:
469–476.
Bengtsson, J., 1987. Competitive dominance among Cladocera:
are single-factor explanations enough? An examination of the
experimental evidence. Hydrobiologia 145: 245–257.
Bogdan, K. G. & J. J. Gilbert, 1987. Quantitative comparison of
food niches in some freshwater zooplankton: a multi-tracer-cell
approach. Oecologia 72: 331–340.
Bohannan, B. J. M. & R. E. Lenski, 1999. Effect of prey heterogeneity on the response of a model food chain to resourceenrichment. Am. Nat. 153: 73–82.
Brooks, J. L. & S. I. Dodson, 1965. Predation, body size, and
composition of plankton. Science 150: 28–35.
Chase, J. M., 1999. Food web effects of prey size refugia: Variable
interactions and alternative stable equilibria. Am. Nat. 154: 559–
570.
134
DeMott, W. R., 1989. The role of competition in zooplankton succession. In Sommer, U. (ed.), Plankton Ecology: Succession in
Plankton Communities. Springer-Verlag, New York: 195–252.
Dodson, S. I., 1970. Complementary feeding niches sustained by
size-selective predation. Limnol. Oceanogr. 15: 131–137.
Gliwicz, Z. M. & W. Lampert, 1990. Food thresholds in Daphnia species in the absence and presence of blue-green filaments.
Ecology 71: 691–702.
Gliwicz, Z. M. & J. Pijanowska, 1989. The role of predation in
zooplankton succession. In Sommer, U. (ed.), Plankton Ecology: Succession in Plankton Communities. Springer-Verlag,
New York: 253–295.
Gliwicz, Z. M. & E. Seidlar, 1980. Food size limitation and algae
interfering with food collection in Daphnia. Arch. Hydrobiol. 88:
155–177.
Goulden, C. E., L. L. Hornig & C. Wilson, 1978. Why do large
zooplankton species dominate? Int. Ver. Theor. Angew. Limnol.
Verh. 20: 2457–2460.
Goulden, C. E., L. L. Henry & A. J. Tessier, 1982. Body size, energy
reserves, and competitive ability in three species of cladocera.
Ecology 63: 1780–1789.
Hall, D. J., W. E. Cooper & E. E. Werner, 1970. An experimental
approach to the production dynamics and structure of freshwater
animal communities. Limnol. Oceanogr. 15: 839–928.
Healey, F. P. & L. L. Hendzel, 1976. Physiological indicators of
nutrient deficiency in lake phytoplankton. Can. J. Fish. aquat.
Sci. 37: 442–453.
Hrbacek, J., M. Dvorakova, V. Korinek & L. Prochazkova, 1961.
Demonstration of the effect of the fish stock on the species
composition of zooplankton and the intensity of metabolism of
the whole plankton association. Int. Ver. Theor. Angew. Limnol.
Verh. 14: 192–195.
Kerfoot, W. C., C. Levitan & W. R. DeMott, 1988. Daphniaphytoplankton interactions: density-dependent shifts in resource
quality. Ecology 69: 1806–1825.
Knisely, K. & W. Geller, 1986. Selective feeding of four zooplankton species in natural lake phytoplankton. Oecologia 69:
86–94.
Lynch, M., 1978. Complex interactions between natural coexploiters – Daphnia and Ceriodaphnia. Ecology 59: 552–564.
Lynch, M., 1979. Predation, competition, and zooplankton community structure: an experimental study. Limnol. Oceanogr. 24:
253–272.
McCauley, E. & F. Briand, 1979. Zooplankton grazing and phytoplankton species richness: field tests of the predation hypothesis.
Limnol. Oceanogr. 24: 243–252.
McCauley, E., 1984. The estimation of the abundances and biomass
of zooplankton in samples. In Downing, J. A. & F. Rigler (eds),
A Manual on the Methods for the Assessment of Secondary
Productivity in Freshwaters. Blackwell Scientific Publications,
Oxford: 228–265.
McCauley, E., W. W. Murdoch & S. Watson, 1988. Simple models
and variation in plankton densities among lakes. Am. Nat. 132:
383–403.
Mittelbach, G. G., A. M. Turner, D. J. Hall, J. E. Rettig & C. W.
Osenberg, 1995. Perturbation and resilience: a long-term, wholelake study of predator extinction and reintroduction. Ecology 76:
2347–2360.
Moore, M. & C. Folt, 1993. Zooplankton body size and community
structure: effects of thermal and toxicant stress. Trends Ecol.
Evol. 8: 178–183.
Morin, P. J., 1987. Salamander predation, prey facilitation, and seasonal succession in microcrustacean communities. In Kerfoot,
W. C. & A. Sih (eds), Predation: Direct and Indirect Impacts
on Aquatic Communities. University Press of New England,
Hanover: 174–187.
Murdoch, W. W., M. A. Scott & P. Ebsworth, 1984. Effects of
the general predator Notonecta (Hemiptera) upon a freshwater
community. J. anim. Ecol. 53: 791–808.
Neill, W. E., 1975a. Experimental studies of microcrustacean competition, community composition, and efficiency of resource
utilization. Ecology 56: 809–826.
Neill, W. E., 1975b. Resource partitioning by competing microcrustaceans in stable laboratory microecosystems. Int. Ver. Theor.
Angew. Limnol. Verh. 19: 2885–2890.
Pace, M. L., K. G. Porter & Y. S. Feig, 1983. Species- and agespecific differences in bacterial resource utilization by two cooccurring cladocerans. Ecology 64: 1145–1156.
Pastorak, R. A., 1981. Prey vulnerability and size selection by
Chaoborus larvae. Ecology 62: 1311–1324.
Reynolds, C. S., 1984. The Ecology of Freshwater Phytoplankton.
Cambridge University Press, Cambridge, U.K.
Richman, S. & S. I. Dodson, 1983. The effect of food quality on
feeding and respiration by Daphnia and Diaptomus. Limnol.
Oceanogr. 28: 948–956.
Romanovsky, Y. E. & I. Y. Feniova, 1985. Competition among
Cladocera: effect of different levels of food supply. Oikos 44:
243–252.
Scott, M. A. & W. M. Murdoch, 1983. Selective predation by the
backswimmer, Notonecta. Limnol. Oceanogr. 28: 352–366.
Sommer, U., M. Gliwicz, W. Lampert & A. Duncan, 1986. The
PEG-model of seasonal succession of planktonic events in fresh
waters. Arch. Hydrobiol. 106: 433–471.
Spitze, K., 1985. Functional response of an ambush predator:
Chaoborus americanus predation on Daphnia pulex. Ecology 66:
938–949.
Steiner, C. F., 2001. Seasonal succession and variable Daphnia
dominance in fishless ponds: ecological determinants and ecosystem consequences. Doctoral Dissertation, Michigan State
University, East Lansing, MI, U.S.A.
Steiner, C. F., 2002. Context-dependent effects of Daphnia pulex
on pond ecosystem function: observational and experimental
evidence. Oecologia 131: 549–558.
Sterner, R. W. & D. O. Hessen, 1994. Algal nutrient limitation and
the nutrition of aquatic herbivores. Ann. Rev. Ecol. Syst. 25: 1–
29.
Swift, M. C. & A. Y. Fedorenko, 1975. Some aspects of prey capture
by Chaoborus larvae. Limnol. Oceanogr. 20: 418–425.
Tessier, A. J. & C. E. Goulden, 1987. Cladoceran juvenile growth.
Limnol. Oceanogr. 32: 680–686.
Tessier, A. J. & J. Welser, 1991. Cladoceran assemblages, seasonal succession and the importance of a hypolimnetic refuge.
Freshwat. Biol. 25: 85–93.
Tillmann, U. & W. Lampert, 1984. Competitive ability of differently
sized Daphnia species: an experimental test. J. Freshwat. Ecol.
2: 311–323.
Vanni, M. J., 1987. Effects of nutrients and zooplankton size on the
structure of a phytoplankton community. Ecology 68: 624–635.
Vinyard, G. L. & R. A. Menger, 1980. Chaoborus americanus
predation on various zooplankters: functional response and behavioral observations. Oecologia 45: 90–93.
von Ende, C. N., 1993. Repeated-measures analysis: growth and
other time-dependent measures. In Scheiner, S. M. & J. Gurevitch (eds), Design and Analysis of Ecological Experiments.
Chapman and Hall, New York: 113–137.
Welschmeyer, N. A., 1994. Fluorometric analysis of chlorophyll
a in the presence of chlorophyll b and phaeopigments. Limnol.
Oceanogr. 39: 1985–1992.