Notes 419
tween heterotrophic protozoa and bacterioplankton
in estuarine water analyzed with selective metabolic
inhibitors. Mar. Ecol. Prog. Ser. 32: 169-179.
- - AND T. BERMAN. 1983. Grazing, growth,
and ammonium excretion by a heterotrophic micro-
flagellate fed with four species of bacteria. Appl. En-
viron. Microbial. 45: 1196-l 20 1.
- -,ANDR.D.FALLON. 1987. Useofmono-
dispersed fluorescently labelled bacteria to estimate
in situ protozoan bacterivory. Appl. Environ. Micro-
biol. 53: 958-965.
SHERR,E. B., F. RASSOIJLZADEGAN,AND B. F.SHERR. 1989.
Bacterivory by pelagic choreotrotrichous ciliates in
coastal waters of the NW Mediterranean Sea. Mar.
Ecol. Prog. Ser. 55: 235-240.
SIEBURTH,J. McN. 1984. Protozoan bacterivory in pe-
lagic marine waters, p. 405-444. Zn J. E. Hobbie and
P. J. 1eB. Williams [eds.], Heterotrophic activity in
the sea. Plenum.
SOL~RZANO,L. 1969. Determination of ammonia in nat-
Limnol. Oceanogr., 39(Z), 1994,419-424
0 1994, by the American Society of Limnology and Oceanography,
Cladoceran body size and vulnerability
Abstract- We examined species-related and age-
related mortality caused by a predaceous copepod
(Acanthocyclops robustus) in five closely related cla-
docerans representing a wide spectrum of body size.
Animals of all five species from clonal cultures were
exposed for 1, 2, or 4 d in medium from a copepod-
infested enclosure that either did or did not contain
natural densities of Acanthocyclops adults and co-
pepodites (40-50 copepods liter-‘). In each of the
five species, the l-d-old neonates were most, and
adults least, vulnerable to the copepods. Small-bod-
ied Daphnia cucullata and Ceriodaphnia reticulata
remained vulnerable until maturation, but the sus-
ceptibility of large Daphnia magna drastically de-
creased in 3- and 5-d-old animals, and 7-d-old adults
were immune to copepod predation.
Size-selective predation by fish and inver-
tebrates has long been considered to play an
important role in structuring zooplankton
populations and communities by selective re-
moval of large-bodied or small-bodied prey.
Although the structuring role of fish predation
has been confirmed by many field and exper-
Acknowledgments
We thank Winfried Lampert, Stephen Wickham, and
two anonymous reviewers for comments on an earlier ver-
sion of the manuscript. Maren Volquardsen provided
technical assistance.
ural waters by the phenolhypochlorite method. Lim-
nol. Oceanogr. 14: 799-801.
STOECKER,D. K., AND G. T. EVANS. 1985. Effects of
protozoan herbivory and carnivory in a microplank-
ton food web. Mar. Ecol. Prog. Ser. 25: 159-167.
TREMAINE,S. C., AND A. L. MILLS. 1987. Inadequacy of
the eucaryote inhibitor cycloheximide in studies of
protozoan grazing on bacteria at the freshwater-sed-
iment interface. Appl. Environ. Microbial. 53: 1969-
1972.
VERITY, P. G. 1985. Grazing, respiration, excretion, and
growth rates oftintinnids. Limnol. Oceanogr. 30: 1268-
1282.
WHEELER,P. A., AND D.L. KIRCHMAN. 1986. Utilization
of inorganic and organic nitrogen by bacteria in ma-
rine systems. Limnol. Oceanogr. 31: 998-1009.
Submitted: 19 August 1992
Accepted: 21 July 1993
Amended: 12 August 1993
Inc.
to copepod predation
imental data (see Hall et al. 1976; Bengtsson
1987) the role of invertebrate predation has
remained in question since it was first sug-
gested by Dodson (1974). Most experimental
evidence for the importance of invertebrate
predation is less compelling than it is for fish
(see Zaret 1980).
Of many different morphological, behavior-
al, and life-history features, body size seems
to be the most important factor responsible for
the vulnerability of zooplankton prey to pre-
dation. This notion is particularly clear in re-
spect to fish predation, which seems evident
from each major review of the subject (Zaret
1980; Kerfoot and Sih 1987; Lazarro 1987).
It is less clear, however, when predation by
invertebrates is reviewed, because other mor-
phological and behavioral features of prey are
often suggested to be more important than prey
body size to various invertebrate predators,
including predaceous copepods.
Although some field and laboratory exper-
iments show that prey body size may be im-
portant to Calanoid copepods such as Diap-
tomus shoshone (Anderson 1970; Dodson
1974) and cyclopoid copepods such as Acan-
thocyclops viridis (Smyly 19 70) or Mesocyclops
edax (Confer 197 1; Brand1 and Fernando 1975;
420
Table 1. Ages at maturation (first clutch released) and
body sizes of five daphnids at the instars used for the
experiments: l-d-old neonates, 3- and 5-d-old juveniles,
and adult 7-d-old females.
Mean
Age l-d
old
(4
Daphnia magna 6.1 1.68
Daphnia pulicaria 6.2 1.01
Daphnia hyalina ‘6.2 0.75
Daphnia cucullata 5.6 0.51
Ceriodaphnia
reticulata 5.0 0.44
* From the upper edge of the eye to the base of the tail spine.
Williamson 1986) vulnerability to predation
by copepods was suggested to be more depen-
dent on other morphological and behavioral
features that are unrelated to body size. Prey
body shape, its external cover, and mode of
swimming were found to be more important
than prey body size to predaceous copepods
such as Acanthocyclops vernalis (Li and Li
1979), Cyclops bicuspidatus (Stemberger and
Evans 1984), and M. edax (Williamson 1983).
Most of the experiments cited above were
done with natural prey densities. Thus, differ-
ent prey species were offered in different den-
sities. The predator was therefore faced not
only with different individual prey vulnera-
bility, but also with different chances of prey
encounter and a choice of selecting more or
less abundant prey. The exception was Kerfoot
(1977) who exposed the same initial densities
of three prey species to known numbers of
Epischura nevadensis. We used a similar ap-
proach in our study: equal numbers of different
cladoceran prey species were exposed to nat-
ural densities of a predaceous copepod in its
natural medium from which the same prey
species had been nearly extinct due to intense
predation by the copepod.
We tested the vulnerability of various in-
stars of five differently sized congeneric cla-
docerans to predation by offering equal num-
bers of various closely related species to
Acanthocyclops robustus (G. 0. Sars) in its nat-
ural medium and its natural densities of 40-
60 copepods liter- l. The five prey species rep-
resented a wide spectrum of body sizes (Table
1) and, except for Ceriodaphnia reticulata,
similar morphology and behavior. Different
body size-related vulnerability of the five cla-
Notes
docerans to predation by A. robustus was al-
ready apparent from a long-term enclosure
study in which the smallest species (C. reticu-
lata and Daphnia cucullata) were exterminat-
body length (mm)* ed by natural densities of the copepod, while
3-d 5-d l-d large-bodied species (such as Daphnia magna
old old old
and Daphnia pulicaria) coexisted with the co-
1.96 2.24 2.52 pepod for 3 months. Each population was in
1.32 1.64 1.96 a peculiar age structure with old individuals
1.02 1.29 1.57
0.66 0.81 0.96
overwhelmingly dominant and neonates near-
ly absent (Gliwicz and Lampert 1993).
0.50 0.56 0.62 All experimental prey animals came from
long-established clones maintained in P&n in
membrane-filtered (0.45 pm) lake water and
fed small green alga (Scenedesmusacutus) from
a chemostat culture. All animals were accli-
mated to the experimental temperature of 14°C.
A cohort of 120-240 synchronized individuals
of each species was prepared for each batch or
flow-through experiment from the offspring re-
leased by egg-carrying females that had been
kept isolated for 12 h.
At the beginning of each batch experiment,
8-l 2 randomly selected individuals of each
species were pipetted into 1.2-liter glass bottles
filled with natural medium from one of the
three copepod-infested enclosures-three con-
trol and three treatment bottles in each exper-
iment. Each bottle contained all five species,
40-60 animals. All bottles were randomly filled
with the natural medium from the enclosure
after mixing its 1.7-m3 volume: the control
bottles with water screened on lOO+m-mesh-
size net to eliminate copepods, the treatment
bottles with unscreened water. A few large
Daphnia flushed accidentally into the treat-
ment bottles were removed by pipet before
experimental prey animals were introduced.
Experimental bottles were kept for 24 or 48
h on a plankton wheel (1 rpm) in dim light at
14°C (the mean enclosure temperature at the
time the experiments were performed, 17 Oc-
tober-20 November 1990). The density of A.
robustus adults and copepodites IV and V at
that time was constant in the copepod-infested
enclosures, which ensured similar predator
densities in experimental bottles (40-60 co-
pepods liter- l, Table 2).
For one experiment with 6-d-old prey ani-
mals, we used a flow-through system (Stich
and Lampert 1984) with a high concentration
(0.5 mg C liter-l) of Scenedesmus as food for
Daphnia. The same number of 12 randomly
 Notes 421

selected synchronized individuals of each spe- Table 2. Experimental protocol, including mean num-
cies were kept for 96 h in six experimental 0.3- bers (+ 1 SD) of the predator (Acanthocyclops robustus
adults and copepodites IV and V) per experimental bottle
liter chambers-again all five species together. (exp. l-4) or flow-through chamber (exp. 5) at the end of
The chambers had been previously filled with experiment (NJ, numbers and age of each of the three
the natural enclosure water with (treatment) or (exp. 1) or five (exp. 2-5) prey species (Daphnidae), those
without (control) A. robustus: three chambers introduced into each replicate bottle or chamber (N,), and
each. those present in treatment bottles at the end of each ex-
periment (N,, mean for all five species, except for exp. 1
At the end of each batch and flow-through in which Ceriodaphnia reticulata and Daphnia magna were
experiment, all prey animals and copepods not used and mean for the three other species is given).
from each replicate were screened on 100~pm
A. robustus
mesh-size net, killed with Formalin, and N Daphnidae
Dura-
counted. For each prey species and each rep- Start tion CIV Age
licate, we calculated death rate as d = (In N, Exp. date 0-4 Adults and CV NO N Cd)
- In NJ/t, where No is the number of intro- 1 17 Ott 24 23(2) 14(3) 8 5.1 1
duced animals, N, is the number of animals 1 17 Ott 48 21(2) 21(5) 8 3.6 1
surviving until the end of experiment, and t is 5 20 Nov 96 24(3) 47(3) 16-53* 1
time in days. The effect of copepod predation 2 9 Nov 24 21(5) 24(2) 10 6.9 3
2 9 Nov 48 21(3) 24(3) 10 6.2 3
was assumed to be the difference between d in 4 16 Nov 24 20(2) 36(3) 10 8.0 5
the treatment individual replicate and the mean 4 16 Nov 48 22(5) 39(3) 10 8.5 5
d from the three reference replicates. Death 5 20 Nov 48 24(3) 37(3) 12 6.6 6
rates never exceeded 0.1 per day in the refer- 3 13 Nov 24 22(2) 35(3) 10 8.6 7
3 13 Nov 48 21(3) 41(3) 10 7.8 7
ence treatment. 1 24 23(2) 14(3)
17 Ott 5 4.2 9
The A. robustus daily feeding rate was cal- 1 17 Ott 48 21(2) 21(5) 5 3.6 9
culated as the sum of F for all five (or three as * Number of neonates born in flow-through chambers to C. retaduta and
in Exp. 1) individual prey species introduced, Duphnra hyulrna during the experiment. These numbers were too low and
too variable in other species to be used to estimate death rate.
F = (NO - NJ/t.
During the flow-through experiment that
lasted 4 d, the prey animals matured and re- D. pulicaria), but they do differ between the
produced. At the end of the experiment, the smallest and the intermediate and between the
offspring of C. reticulata and Daphnia hyalina intermediate and the largest D. magna: differ-
that were already 10-d old were numerous ences among adjusted means were significant
enough in the treatment and the experimental at P II 0.0001 (F = 43, df = 66) and P 5 0.002
chambers to calculate the effect of copepod (F = 10.6, df = 57) respectively (ANCOVA).
predation in a slightly different way by assum- Each of the two patterns stems from the same
ing that the numbers of neonates born in each relation, which seems to be independent of
treatment chamber were equal to the mean other species-specific characteristics than body
numbers of neonates surviving to the end of size. This relation between vulnerability to co-
the experiment in the reference chambers. pepod predation and cladoceran prey body size
These data have been arbitrarily treated as data becomes more apparent when individual age
for 1-d-old prey individuals. is replaced by body length, which allows us to
Two clear patterns can be seen (Fig. 1). First, pool the data for all instars of all five prey
in each species, the neonates are most affected species (Fig. 3).
by A. robustus and vulnerability to the copepod The A. robustus feeding rate (calculated as a
predation significantly decreases in older in- difference in the mean final numbers of all five
stars (the slopes of all regressions are different prey species in the treatment and the reference
from 0, see Fig. I). replicates; Table 2) was between 0.06 and 0.24
Second, individuals of corresponding age are prey copepod-l d-l in batch experiments with
more vulnerable in small-bodied than in large- grown 9-d-old adults (48 h) and small-bodied
bodied species (Fig. 2). Neither the slopes nor l-d-old neonates (24 h). These values are in
the adjusted means of death rate on age re- the range of feeding rates that have been re-
gressions (Fig. 1) differ among the two smallest ported for other predaceous cyclopoid cope-
species (C. reticulata and D. cucullata) or pods of similar size ( 1.2-l .6-mm body length)
among the two intermediates (D. hyalina and feeding on small-bodied cladocerans (offered
422 Notes

:ik C. rticulata

I I- 4 6 8 IO
D. cucullata
m

individual age (days)

Fig. 2. Summary of data from Fig. 1: mean values for
4 6 8 10 different instars of five prey cladocerans.

D. hyalina
$ 0.8- in much higher densities): e.g. 0.02-0.1 prey
; 0.6 copepod-l d-l in C. bicuspidatus fed Cerio-
5 0.4 daphnia sp. (McQueen 1969), 0.3-0.4 in Cy-
clops vicinus fed C. reticulata (Brand1 and Fer-
c 0.2 nando 1975), and 0.2-0.6 in C. vicinus and
3 0
2i Cyclops kolensis fed D. cucullata and D. hy-
alina (Santer 1990).
1 D. pulicaria In each of the works cited above, feeding
0.8 rate was shown to decrease with prey body size.
Santer (1990) found that feeding rate was 3
times higher when the copepods were fed with
D. hyalina 0.7-mm neonates than when they
were fed with 1.8-mm adult females. This find-
ing corresponds with our data in Fig. 3 which
0 2 4 6 8 10 displays similar differences in death rates in
D. hyalina 0.75-mm neonates and 1.83-mm
D. magna 9-d-old females. These rates are 0.294 d-l
(kO.211) and 0.036 d-l (*0.029), mean (+ 1
SD), respectively.
Our data show that copepods may play an
0.2- - important role in limiting densities of cladoc-
eran populations, particularly when fish are
O-rlT-e~---- absent, as could be seen in our enclosure study
-0 2 4 6 8 10
(Gliwicz and Lampert 1993), in the alpine West
Individual age (days) Elk Mountain ponds of Dodson (1974), and
Fig. 1. Data on death rates resulting from copepod in alpine lakes free of fish in the Tatra Moun-
predation in different instars of five prey cladoceran species tains (Gliwicz and Rowan 1984). In most fish-
exposed to Acanthocyclops for 24 h (H), 48 h (Q, and 96
h (El). The slopes of all death rates on individual age re-
less Tatra lakes, the dominant cladoceran is
gression lines are different from 0 with P I 0.005. n and the large D. pulicaria and the dominant co-
F for the five species: 24 and 22.2, 33 and 28.1, 36 and pepod is the large Cyclops abyssorum. For most
17.7, 36 and 16.4, 24 and 16.6, from the smallest Cerio- of the year, the age structure of the D. pulicaria
daphnia reticulata) to the largest (Daphnia magna). For population is similar to that from our cope-
the two small and the three large-bodied prey species, the
slopes are also different from each other (adjusted means pod-infested enclosures: large, old females are
different at P I 0.002, ANCOVA). The 24-h and 48-h overwhelmingly dominant. In all the Tatra
data are shifted for clarity 0.1 d left and right, respectively. lakes stocked with fish, D. pulicaria disap-
 Notes 423

Cr DC Dh Dp Dm

Log body length (mm)

Fig. 3. Data from Fig. 1 for all five daphnid prey plotted against log body length assuming that all animals in one
synchronized cohort had the same length (Table 1). Death rates based on log body-length regression lines are given
for all five species. All regression slopes are different from 0 at P < 0.003 (F > 16). For each of the two small and the
three large-bodied prey species, the regression slopes also differ from each other (different adjusted means and different
slopes at P I 0.05, ANCOVA).

peared long ago but has never been replaced
by small-bodied cladocerans (e.g. Bosmina sp.)
that can be found nearby. Is this a deleterious
effect of C. abyssorum which became more
abundant after fish introductions (Gliwicz and
Rowan 1984)? C. abyssorum is even more vo-
racious than other predaceous copepods when
feeding on small cladocerans; its feeding rates
have been shown to exceed 2 prey copepod-’
d-l (Santer 1990).
The importance of copepods in structuring
cladoceran communities and populations is
clearly associated with the body size-related
vulnerability of cladocerans to the deleterious
effects of copepods. Small-bodied species and
early instars are most vulnerable to copepods
in terms of increased mortality risk, as we show
here. There is also, however, another kind of
deleterious effect to which large species and
late instars are more vulnerable. They are vul-
nerable in terms of reduced reproduction; the
first copepodite stages ofA. robustus have been
shown to invade Daphnia brood chambers to
feed on eggs and embryos and to suck materials
from ovaries (Gliwicz and Stibor 1993). The
largest D. magna is most vulnerable. When
grown, its survival is no longer endangered by
copepods, but its reproduction may still be se-
verely affected.
Z. Maciej Gliwicz’
Gerard0 Umana2
Max Planck Institute for Limnology
Postfach 16 5
W-2320 Pliin, Germany
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Laboratory experiments focusing on the po-
tential toxicity of cyanobacteria to planktonic
crustaceans have produced some contradic-
tory results (see Lampert 1987; Paerl 1988; de
Bernardi and Giussani 1990). For instance, in
a study by de Bernardi et al. (198 1) all three
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species. Other studies have compared several
cyanobacterial strains and have shown that
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others are not (Nizan et al. 1986; Vasconcelos
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