Journal of Plankton Research Vol.21 no.8 pp.1553–1564, 1999
Reproductive allocation in Daphnia exposed to toxic
cyanobacteria
Marko Reinikainen1,2,3, Jaana Hietala2 and Mari Walls2
1University of Helsinki, Tvärminne Zoological Station, FIN-10900 Hanko and
2University of Turku, Department of Biology, Section of Ecology, FIN-20014
Turku, Finland
3To
whom correspondence should be addressed at: Umeå University, Department
of Ecology and Environmental Science & Umeå Marine Sciences Centre, S-901 87
Umeå, Sweden
Abstract. We investigated experimentally how resources were allocated to reproduction in Daphnia
pulex and Daphnia longispina when varying levels of toxic Microcystis were added to higher quality
food. We used multiple regression models to estimate mean offspring size and clutch size in relation
to maternal size and clutch number, and analysed effects of treatments on residuals from the models.
We also measured variation in per offspring investment. At a high cyanobacterial level, D.pulex was
virtually unable to reproduce. At a lower level, D.pulex produced small clutches. However, the regression model residuals indicated that the presence of cyanobacteria increased the portion of available
resources allocated to reproduction. The observed allocation may be a means to maximize reproduction under diminished longevity. Effects on mean offspring size were marginal in D.pulex, but
variation in per offspring investment sometimes decreased in cyanobacterial exposures. Daphnia
longispina was affected by a higher cyanobacterial level only, where offspring size was reduced. Deviations from the regression model indicated that effects on maternal size alone do not explain this
effect. Clutch size residuals and per offspring investment were unaffected by treatments in
D.longispina. The observed responses differ from theoretical models on reproductive allocation under
food limitation.
Introduction
The performance and competitive ability of an individual are affected by the way
it allocates resources to reproduction in different environments. It is often
assumed that there is a fixed amount of resources available for reproduction at a
given time of an individual’s life history (Smith and Fretwell, 1974; Ebert, 1994)
and that increased reproductive investment takes place at the cost of somatic
investment [Williams, 1966; see Tuomi et al. (1983) for alternative allocation
systems]. When these assumptions are true, offspring size, offspring number and
maternal size are interrelated parameters that vary within limits set by morphological and other constraints (e.g. Glazier, 1992). The relative importance of these
life history parameters depends on the given environmental conditions. Variation
in food quantity is the most studied environmental parameter in papers concerning reproductive allocation in Daphnia. Small offspring size has, for instance,
been shown to be associated with low starvation resistance (e.g. Threlkeld, 1976;
Tessier et al., 1983; Goulden et al., 1987). Producing large clutches and consequently smaller offspring should, therefore, be advantageous at high food levels
only. According to Smith and Fretwell (1974), it should furthermore be important to invest resources evenly, so that all offspring are close to the size that is
optimal for a given environment.
© Oxford University Press
1553
M.Reinikainen, J.Hietala and M.Walls
It is important to note, however, that reproductive allocation is not affected by
food level only; effects of food quality are equally important (Brett, 1993).
Cyanobacteria are generally regarded as a poor-quality food source, and several
studies have shown that exposure to toxic strains results in markedly reduced
clutch sizes in Daphnia and other zooplankton (e.g. Porter and Orcutt, 1980;
Fulton and Paerl, 1987; Hanazato and Yasuno, 1987; Gilbert, 1990). Effects of
toxic cyanobacteria on offspring quality, however, have not been studied previously. In natural waters, food quality fluctuates as markedly as does food quantity (Sommer et al., 1986). In particular, the often rapid occurrence of
cyanobacteria as a part of the phytoplankton community is believed to have a
negative effect on large cladocerans (e.g. Edmondson and Litt, 1982; Infante and
Abella, 1985; Jarvis et al., 1987). According to Sivonen et al. (1990), ~50% of
dense populations of cyanobacteria are toxic, containing neurotoxic alkaloids
and/or hepatotoxic peptides. Both of these groups of toxins have been shown to
affect Daphnia in laboratory studies (DeMott et al., 1991; Haney et al., 1995).
In this study, we report how a peptide toxin-producing strain of the cyanobacterium Microcystis aeruginosa affects reproductive allocation in Daphnia. Our
study includes several improvements over earlier papers concerning life history
effects of toxic cyanobacteria on Daphnia: (i) we studied both offspring size and
offspring number; (ii) we considered the possibility that maternal size and
reproductive instar affect reproductive allocation (see Glazier, 1992); (iii) we
used five genotypes (clones) of Daphnia, originating from two different species
(Daphnia pulex and Daphnia longispina). The study of different genotypes is
important because interclonal variation in responses is a requisite for selection
(Glazier, 1992; Boersma, 1995). Furthermore, there is large variation in the
susceptibility of different Daphnia clones to toxic substances (Baird et al.,
1990). Therefore, conclusions derived from studies of a single clone may be of
limited value.
Method
Individuals from three clones of D.pulex (P1, P2 and P3) and two clones of
D.longispina (L1 and L2), kept as stock cultures in our laboratory, were used in
the experiment. These clones have been isolated from small, fishless ponds near
Turku in SW Finland. All clones derive from separate ponds. The phytoplankton
composition and other environmental characteristics of the pond habitats are
often unstable (C.Laurén-Määttä, unpublished data), and we will not attempt to
link our results to the history of the Daphnia clones. Experimental animals were
obtained from the second or third clutch of mothers that had been born into the
experimental conditions [see Hietala et al. (1995) for details]. Filtered (Whatman
GF/C) lake water from Lake Littoistenjärvi (SW Finland) was used as Daphnia
medium in all cultures.
The green alga Scenedesmus obtusiusculus was used as food in the Daphnia
cultures, as well as during the experiment. The cyanobacterium used was
M.aeruginosa (strain PCC7820). This cyanobacterial strain produces at least one
variant of cyclic peptide toxins called microcystins. One or more unknown toxins,
1554
Reproductive allocation in Daphnia
that are probably more toxic to Daphnia than microcystins, may also be present
(Reinikainen et al., 1994).
The cyanobacterial treatments consisted of a mixture of 20 000 cells ml–1 of
S.obtusiusculus (0.260 mg C l–1) and 10 000 or 40 000 cells ml–1 of cyanobacteria
(0.076 and 0.304 mg C l–1, respectively). Unexposed control animals were fed
Scenedesmus only. All animals were reared individually in 20 ml vessels, at 20°C,
and on a 16 h:8 h light:dark cycle. They were transferred daily into fresh media.
Ten replicate animals of each clone were used per cyanobacterial treatment and
in the controls. At the beginning of the experiment, the animals were <24 h of age.
As the animals were transferred to fresh treatment media; offspring, if any,
were counted and preserved in 70% ethanol. The preserved offspring were later
measured under a microscope (length from the base of the tail spine to the top
of the compound eye). A mean offspring size and the coefficient of variation (CV)
were calculated for each clutch of each replicate animal. Data on the first three
clutches were included in statistical analyses: clutches that were produced later
were excluded because of the low number of reproducing replicates in cyanobacterial treatments. Preliminary statistical analyses included two-way
MANOVAs, with mean offspring size as dependent variable, and cyanobacteria
and clone as independent variables. Effects on the CVs were analysed using twoway ANCOVAs, with maternal carapace length as a covariate (see e.g. Boersma,
1995).
There is a trade-off between offspring size and number in Daphnia, and these
parameters are also affected by maternal size and clutch number (e.g. Boersma,
1995). Therefore, further analyses were carried out as follows: we used multiple
regression models that included maternal size, clutch number and clutch size to
estimate offspring size. Using stepwise forward selection, variables with P values
of <0.150 were included in final models. Similar regression models were used to
estimate clutch sizes, with offspring size replacing clutch size as one of the regression variables. To investigate how true (observed) values differed from the estimated (predicted) values, residuals from the regression models were calculated.
Effects of treatments were then analysed using two-way MANOVAs. In these
MANOVAs, cyanobacteria and clone were the independent variables, and the
offspring size and clutch size residuals (analysed in separate MANOVAs) for
clutches 1–3 were the dependent variables. The MANOVAs were followed by
two-way ANOVAs on each of the three clutches. Fixed models were used in the
analyses. Interactions and main effects were interpreted from the MANOVA and
ANOVA tables, and visually from graphs, according to Mead (1988).
All data for the two Daphnia species were analysed separately, as D.pulex did
not have enough reproducing replicates at the higher cyanobacterial level to
allow statistical comparisons. SAS Version 6.09 (Statistical Analysis Systems,
1989) was used in the analyses.
Results
The main focus of this study is on the specific relationships between different life
history characteristics. These relationships are presented in the sections below.
1555
M.Reinikainen, J.Hietala and M.Walls
Only a short summary of general treatment effects on these characteristics per se
is given here. This summary is partly based on a previous study on the same data
set (Hietala et al., 1995), where survival, somatic investments and intrinsic growth
rates were the subjects of interest.
As could be expected, maternal growth and clutch sizes were reduced in cyanobacterial treatments [Figure 1A and B; see Hietala et al. (1995) for details]. Clutch
size reductions occurred in D.pulex at the lower concentration, whereas
D.longispina clutches were reduced at the higher concentration only. A statistically significant effect of cyanobacteria on offspring size was observed in
D.longispina only (two-way MANOVA; Wilks’ L: F6,6 = 4.60; P = 0.043). The
other main factor (clone) and the interaction term were not statistically significant. The effect of cyanobacteria was associated with a decrease in offspring size
in clutches 1 and 3 at the higher cyanobacterial level (Figure 1C). The mean CV
of D.pulex offspring size was reduced by the cyanobacteria (Table I). The effect
of cyanobacteria was statistically significant in clutch 3 (ANCOVA; F1,32 = 6.84;
P = 0.01) and the effect of clone in clutch 1 (ANCOVA; F2,43 = 3.39; P = 0.04).
Maternal size, which was used as a covariate, had no effect on this parameter. The
CVs of D.longispina (Table I) were not affected in a statistically significant way.
Offspring size residuals
In the regression model estimating offspring size in D.pulex, the effects of maternal size and clutch number were statistically significant (Table IIA). The clone 3
cyanobacteria interaction in the MANOVA on the offspring size residuals
approached significance (Table IIIA). ANOVAs on the separate clutches showed
that this effect is explained mainly by responses in the second clutch (Table IIIA).
The mean residuals (Figure 2, left panel) imply that the largest difference in the
reactions in clutch 2 is that between clones P2 and P3, with the former clone
producing larger offspring than the model predicts, and the latter one smaller
offspring, when exposed to cyanobacteria. Keeping in mind the high P value in
Table I. Effects of toxic cyanobacteria (Cya) on within-clutch variability in resource investment: the
coefficient of variation for offspring size (length in µm) of D.pulex (clones P1–P3) and D.longispina
(L1 and L2). Treatments consisted of control (0), a low (1) and a high (2) level of cyanobacteria.
Numbers in parentheses indicate the SE
Clone
Cya
Clutch 1
Clutch 2
Clutch 3
P1
0
1
0
1
0
1
0
1
2
0
1
2
2.31 (0.57)
2.05 (0.34)
2.14 (0.26)
1.90 (0.33)
1.63 (0.29)
0.90 (0.12)
4.11 (0.79)
4.39 (0.53)
3.35 (0.78)
6.30 (2.27)
2.91 (0.52)
6.40 (1.92)
1.80 (0.24)
1.24 (0.18)
2.57 (0.33)
1.95 (0.31)
1.82 (0.43)
1.76 (0.43)
3.83 (0.67)
2.08 (0.34)
3.27 (–)
1.96 (0.15)
2.40 (0.50)
3.69 (0.58)
2.14 (0.34)
1.77 (0.59)
2.16 (0.32)
1.81 (0.21)
2.33 (0.35)
1.11 (0.17)
2.24 (0.59)
3.00 (0.28)
5.16 (2.90)
4.44 (1.30)
5.62 (1.77)
3.43 (0.73)
P2
P3
L1
L2
1556
Reproductive allocation in Daphnia
Fig. 1. Mean maternal size (A), clutch size (B) and offspring size (C) of Daphnia. Bars indicate SE.
The plots are for a control treatment, a low cyanobacterial treatment and a high cyanobacterial treatment. Filled symbols are for D.pulex and open symbols for D.longispina. The plots contain pooled
data for three clones of the former species and two of the latter one.
the MANOVA, and the large SEs, this interpretation of the graphs is only
suggestive.
Effects of maternal size were also statistically significant in the regression
model estimating offspring size in D.longispina, whereas effects of clutch number
approached significance (Table IIA). The MANOVA showed that the main
factors clone and cyanobacteria both had statistically significant effects on the
1557
M.Reinikainen, J.Hietala and M.Walls
Table II. Parameter estimates (PE) and their significance levels for regression models on offspring
size (A) and clutch size (B) in D.pulex and D.longispina. The numbers in parentheses indicate the SE
of PE. The variables clutch number and maternal size were included in the regression models, using
stepwise forward selection. The variables clutch size (for the models in A) and offspring size (for the
models in B) were excluded from the final models because of P values > 0.150
Variable
D.pulex
(A)
Intercept
Clutch no.
Maternal size
D.longispina
––––––––––––––––––––––
––––––––––––––––––––––––––
PE
P
PE
P
454.6 (25.8)
9.9 (3.4)
0.1 (<0.1)
r2 = 0.34
<0.001
0.004
<0.001
390.4 (32.4)
7.7 (4.6)
0.1 (<0.1)
r2 = 0.30
<0.001
0.096
<0.001
2.9 (1.6)
2.3 (0.1)
<0.1 (<0.1)
r2 = 0.77
0.014
<0.001
0.004
–9.4 (1.8)
–0.7 (0.2)
<0.1 (<0.1)
r2 = 0.41
<0.001
0.008
<0.001
(B)
Intercept
Clutch no.
Maternal size
Table III. Effects of cyanobacteria (Cya) and clone (Cl) on offspring size in Daphnia: multivariate
(Wilks’ L) and univariate statistics on residuals from multiple regression models that included the
variables maternal size and clutch number. (A) D.pulex; (B) D.longispina
(A)
Source
Cl
Cya
Cl 3 Cya
Wilks’ L
––––––––––––––––––
d.f.
F
P
6, 56
3, 28
6, 56
3.42
1.77
1.89
0.006
0.336
0.098
univ. d.f. Clutch 1a
Clutch 2b
Clutch 3c
F
P
5.27
2.98
0.22
0.012
0.095
0.800
–––––––––– –––––––––– ––––––––––
2
1
2
F
P
F
1.34
0.01
1.95
0.278
0.905
0.160
2.70
0.31
5.61
P
0.083
0.583
0.008
Error 30 (Error MS: a470.1; b577.6; c627.0).
(B)
Source
Cl
Cya
Cl 3 Cya
Wilks’ L
––––––––––––––––––
d.f.
F
P
3, 16
6, 32
6, 32
7.53
5.22
0.86
0.002
0.001
0.537
univ. d.f. Clutch 1a
Clutch 2b
Clutch 3c
F
P
F
P
1.40
1.02
0.13
0.252
0.379
0.880
4.27
0.62
0.02
0.054
0.547
0.980
–––––––––– –––––––––– ––––––––––
F
1
2
2
P
11.30 0.003
15.64 <0.001
2.54 0.107
Error 18 (Error MS: a237.7; b821.4; c1320.4).
residuals (Table IIIB). Univariate statistics revealed that the effect of cyanobacteria is explained by responses in the first clutch (Table IIIB). In that clutch, both
D.longispina clones produced smaller offspring than predicted by the regression
model at the higher cyanobacterial level (Figure 2, right panel; mean of dark bars
~–27). The corresponding value is positive for the lower cyanobacterial level
(mean of striped bars ~18) and ~0 at the control level (mean of empty bars). The
effect of clone is explained by higher mean residuals in clone L2 than in clone L1
in clutches 1 and 3 (Figure 2, right panel).
1558
Reproductive allocation in Daphnia
Fig. 2. Effects of cyanobacterial treatments on mean residuals from regression models predicting
offspring sizes in D.pulex clones P1–P3 and D.longispina clones L1 and L2. Two cyanobacterial levels
are included for D.pulex and three for D.longispina. Bars indicate the SE.
Clutch size residuals
The regression model estimating clutch size in D.pulex revealed that the variables clutch number and maternal size both had a statistically significant effect
on clutch size (Table IIB). There was a statistically significant effect of cyanobacteria on the residuals from the regression model as analysed by MANOVA and
1559
M.Reinikainen, J.Hietala and M.Walls
Table IV. Effects of cyanobacteria (Cya) and clone (Cl) on clutch size in Daphnia: multivariate
(Wilks’ L) and univariate statistics on residuals from multiple regression models that included the
variables maternal size and clutch number. (A) D.pulex; (B) D.longispina
(A)
Source
Cl
Cya
Cl 3 Cya
Wilks’ L
––––––––––––––––––
d.f.
F
P
6, 74
3, 37
6, 74
1.01
4.50
1.45
0.422
0.009
0.208
univ. d.f. Clutch 1a
Clutch 2b
Clutch 3c
F
F
–––––––––– –––––––––– ––––––––––
F
2
1
2
P
0.07 0.930
10.91 0.002
1.40 0.260
0.11
9.95
0.60
P
0.892
0.003
0.555
P
1.39 0.260
13.54 <0.001
0.17 0.848
Error 39 (Error MS: a0.91; b0.83; c1.32).
(B)
Source
Cl
Cya
Cl 3 Cya
Wilks’ L
––––––––––––––––––
d.f.
F
P
3, 25
6, 50
6, 50
0.22
0.37
1.54
0.885
0.892
0.713
univ. d.f. Clutch 1a
Clutch 2b
Clutch 3c
F
P
0.02
0.85
0.20
0.885
0.439
0.824
–––––––––– –––––––––– ––––––––––
1
2
2
F
P
F
0.29
0.26
2.74
0.597
0.770
0.082
0.40
0.03
1.76
P
0.530
0.967
0.191
Error 27 (Error MS: a3.52; b3.12; c3.24).
subsequent univariate statistics (Table IVA). All clutches from exposed animals
were larger than the model predicts, whereas control clutches were smaller
(Figure 3, left panel).
Clutch size residuals (Figure 3, right panel) in D.longispina were not affected
by the treatments in a statistically significant way (Table IVB). In the regression
model, the effects of maternal size and clutch number were significant (Table
IIB).
Discussion
Our intention to study relationships between reproductive allocation and other
life history characteristics in Daphnia under different food conditions was not
facilitated by differences between clones and subsequent clutches. However,
some potentially important observations emerged.
Regarding offspring size, we observed that one of the species used
(D.longispina) was able to reproduce at a high cyanobacterial level, but that the
size of the neonates was reduced. The reductions were of the order of 5–10%
(Figure 1C). Brett (1993) also demonstrated maternally mediated effects, which
were caused by M.aeruginosa. These effects were persistent, and a ~5% reduction in size correlated with smaller clutch sizes, an increase in age at maturity and
decreased instantaneous population growth rates. Thus, even small reductions in
size can be biologically important. Decreased offspring size has also been demonstrated by Repka (1997, 1998), who used a strain of the cyanobacterium Oscillatoria limnetica. In the latter study of Repka, effects were statistically significant
even after corrections for maternal size (which also had a significant effect).
1560
Reproductive allocation in Daphnia
Fig. 3. Effects of cyanobacterial treatments on mean residuals from regression models predicting
clutch sizes in D.pulex clones P1–P3 and D.longispina clones L1 and L2. Two cyanobacterial levels
are included for D.pulex and three for D.longispina. Bars indicate the SE.
Likewise, maternal size alone did not explain the responses in our experiment,
because residuals from the regression models were also affected (Table IIIB).
Possibly, D.pulex offspring were also affected after corrections for maternal
size and clutch number, because a weak clone 3 cyanobacteria interaction was
observed (Table IIIA). Unfortunately, this interaction was only found in one
1561
M.Reinikainen, J.Hietala and M.Walls
clutch, and interpretations regarding consequences for the relative fitness of the
clones under stress from cyanobacteria cannot be made from these data (but see
Hietala et al., 1995).
The present study suggests that toxic or low-quality food can cause concurrent
reductions in offspring and clutch size. This result is in accordance with the earlier
studies by Brett (1993) and Repka (1997, 1998), in which cyanobacteria were used
as low-quality food, but toxicity was not known. In contrast, studies on relationships between low food quantity and reproductive allocation have shown that
similar reductions in clutch size as those we observed correlate with increases in
offspring size (e.g. Glazier, 1992; Ebert, 1994; McKee and Ebert, 1996). These
increases are believed to be adaptive responses that result in large offspring with
a high resistance against food shortage. We suggest that toxicity or other
unfavourable biochemical properties in food give rise to differing, non-adaptive
responses, caused by disturbed egg development. This suggestion is in accordance
with an earlier report on decreased egg viability in Daphnia exposed to toxic
Microcystis (Reinikainen et al., 1995).
An opposing view would be that reductions in offspring size as a response to
cyanobacteria are adaptive. This view is contradicted by the results of Brett
(1993): larger offspring born from mothers fed high-quality food did better than
smaller offspring produced by mothers fed Microcystis, when reared on a cyanobacterial diet. Adaptive responses to highly variable biochemical properties of
different phytoplankton may be generally less common than those produced by
a more uniform selection pressure such as food limitation, which is at least
temporally common in many environments.
A final note on offspring size concerns per offspring investments. According to
Tessier and Consolatti (1989), variability in offspring size can be explained by
problems associated with fractional resource allocation. Large variance is often
the result of one small juvenile [but see Ebert (1994)], for which there has not
been enough resources, and this is especially true in small clutches. Therefore,
theoretical predictions of even offspring sizes (Smith and Fretwell, 1974) are not
always valid in small clutches. We expected increasing within-clutch variation in
cyanobacterial exposures because clutch size decreased. If anything, there was a
decrease in CV in D.pulex (Table I), which was statistically significant in one
clutch. Possibly, abortions in cyanobacterial exposures (Reinikainen et al., 1995)
could remove small eggs, which, according to Bell (1983), do not always hatch.
Thus, measuring eggs instead of juveniles could have given more information on
the subject.
Regarding relationships between clutch size and other life history parameters,
we note that there were consistent treatment effects on the residuals from the
regression models in D.pulex (Table IVA). The response to cyanobacteria was,
in each clutch of all clones, an increased clutch size relative to the estimates of
the model (Figure 3, left panel). (Note that this interpretation concerns the
residuals, not the actual clutches, the size of which decreased in exposures; Figure
1B.) At present, we do not know whether there is an evolutionary reason for this
phenomenon. One such reason could be that under conditions which do not
permit long survival and the production of several clutches, it is favourable to
1562
Reproductive allocation in Daphnia
allocate all available resources to reproduction. A problem with this explanation
is that reproduction should then occur earlier than in an environment with low
mortality risk. In reality, reproduction was delayed in exposures (Hietala et al.,
1995). Possibly, D.pulex growth was delayed due to toxic stress, but when the
animals were large enough, reproduction was favoured over size. The question
remains whether D.pulex can actually sense that exposure to cyanobacteria
constitutes a high mortality risk. It is also not clear why D.longispina did not show
a consistent response pattern.
Acknowledgements
We are indebted to Camilla Laurén-Määttä and Matti Ketola, who made valuable suggestions on data interpretation. This study was supported by grants from
the Academy of Finland to M.R. (Academy of Finland grants 7685 and 42768)
and M.W., and from the Maj and Tor Nessling Foundation. This work is also part
of University of Helsinki programme number 98524002.
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Received on January 5, 1997; accepted on April 22, 1999
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