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Reference:
Biol.
Bull.
176:147—154.
(April,
1989)
The Effect of Hydra on the Outcome of Competition
Between Daphnia and Simocephalus
STEVEN S. SCHWARTZ AND PAUL D. N. HEBERT
Department ofBiological Sciences, University of Windsor, Windsor, Ontario, Canada N9B 3P4
Abstract. The cladoceran genera Daphnia and Simo
cephalus often co-occur in nature. In laboratory experi
ments, populations ofthe two genera had similar growth
rates when grown separately, but when cultured together
Daphnia invariably excluded Simocephalus. However,
the added presence of the littoral zone predator, Hydra,
reversed this trend with Simocephalus remaining after
Daphnia had been eliminated. This result was robust in
culture vessels as small as 100 ml and as large as 85 1.It
is hypothesized that Simocephalus has evolved a suite of
energetically expensive traits to deter littoral zone preda
tors, whereas Daphnia, which are pbanktonic, have not
evolved such costly traits and hence have more energy
available for reproduction and are able to exclude Simo
cephalus.
1978; O'Brien and Vinyard, 1978; Cooper and Smith,
1982). When predator pressure is low, the susceptible
morph is able to numerically dominate the protected
morph. While the maintenance of distinct morphs is
striking, predation has also been a significant selective
force in the evolution of previously overlooked charac
teristics which not only reduce predation rates, but
which also effect interactions between prey species.
Schwartz et al. (1983) demonstrated that Hydra are
efficient predators ofthe cbadoceran Daphnia, but rarely
capture members ofthe closely related genus, Simoceph
alus, which inhabit the littoral zone along with Hydra.
Simocephalus has a suite ofcharacteristics that deter pre
dation by Hydra. The evolutionary origin of each trait
is unknown, but may be, in part, the result of selective
pressure by Hydra or other littoral zone predators. The
behavior of Simocephalus is such that it spends most of
the time attached to substrates and is therefore not in the
water column where it might encounter the tentacles of
Hydra. In addition, physiological adaptations allow Si
mocephalus to swim among the tentacles ofHydra with
out eliciting the discharge of nematocysts. Finally, when
nematocysts are discharged, Simocephalus is unharmed,
suggesting that the nematocysts fail to penetrate this cla
doceran's heavy carapace. In contrast, Daphnia, which
is pbanktonic, is highly vulnerable to predation by Hydra.
One explanation for the vulnerability ofDaphnia is that,
because Daphnia rarely encounters Hydra, it has failed
to evolve mechanisms that reduce the impact ofthe pred
ator.
Is there a cost to Simocephalus associated with its suite
of anti-predator adaptations? Competition experiments
between Daphnia and Simocephalus have invariably
shown that Daphnia outcompetes its relative (Frank,
Introduction
Over evolutionary time prey species have limited the
impact of predation by behavioral, physiological, and
morphological adaptations (Sih, 1987). The conse
quences of these adaptations are not restricted to the
predator-prey relationship, but may also be important in
other facets ofthe ecology ofthe prey species. For exam
pbe, morphological features of many planktonic cladoc
erans not only deter predation, but also effect competi
tive interactions. Predator-resistant morphs of Bosmina
and Ceriodaphnia are competitively inferior to predator
susceptible morphs (Nibssen et al., 1980; Zaret, l972a;
b). The maintenance ofsuch morphological diversity has
been termed predator balanced polymorphism (Zaret,
1969). The energetic cost ofpredator deterrence is appar
ently reflected in reduced fecundity and consequently re
duced competitive ability (Kerfoot, 1975, 1977; Jacobs,
Received l7July 1987;accepted3Oianuary
1989.
1952;
Corigliano
and
de
Bernardi,
1978;
de
Bernardi
147
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and
148
S. S. SCHWARTZ AND P. D. N. HEBERT
Manca, 1981; 1982; Crowley and Johnson, 1983). In
general, these studies indicate that Simocephalus has a
lower intrinsic rate of increase than Daphnia and this
rate is additionally reduced by the presence of the com
petitor. The results of these competition experiments
have been explained by proximate differences in life his
tory characteristics, without attempting to examine the
ultimate factors that have selected these suites of traits.
The robeofpredation has, for instance, been neglected in
explanations ofthe relative position ofthe two genera in
a competitive hierarchy.
In this paper we show that the outcome of laboratory
competition experiments between Daphnia and Simo
cephalus can be altered by the presence ofa predator that
consistently selects the prey species that has not been ex
posed to selective pressures favoring the evolution of ap
propriate defensive tactics. We suggest that the reduced
competitive ability of Simocephalus as compared to
Daphnia is largely the result of energetically expensive
anti-predator adaptations required for life in the littoral
zone.
Materials and Methods
The effect of Hydra oligactis predation on the out
come ofcompetition between Daphnia pulex and Simo
cephalus vetulus, two commonly co-occurring cladocer
ans, was evaluated in three sets of laboratory experi
ments. Both cladoceran species and the Hydra were
cbonal populations (Daphnia pulex clone Wi-i) main
tamed in the laboratory and originally collected in the
Windsor, Ontario, area. Experiments were initiated in
synthetic pond water (Hebert and Crease, 1980), but this
was gradually replaced during the experiments with con
ditioned tap water containing algal food. All experiments
were conducted at 15°C
and 12:12 LD. During the exper
iments the cladocerans were fed at two-day intervals with
a mixed algal culture, primarily Scenedesmus sp., main
tamed in the laboratory. No attempt was made to quan
tify the feeding regime as all experiments were conducted
concurrently; i.e., all vessels in an experiment received
the same amount and quality offood. As control popula
tions showed a rapid numerical increase (Figs. 1, 4), it
was assumed that the feeding regime was adequate.
The first two experiments were similar in design,
differing primarily in the size of the vessel used. In one
set ofexperiments, 120 ml plastic cups were filled to 100
ml. Each treatment was replicated in triplicate. Oviger
ous females were used to initiate each replicate cup. Con
trol cups received six individuals from one of the two
cladoceran species. Competition cups were initiated with
three individuals from each species. Additional competi
tion cups were also set up with six D. pulex and three
S. vetulus to determine
if Daphnia would more quickly
outcompete Simocephalus under these conditions. The
impact of a selective predator, Hydra, was determined
in another set of competition cups (initiated with three
females from each species) as well as control cups (with
six individuals of each species), with each cup receiving
one adult Hydra, without buds. All individuals were
counted in each cup once a week for five weeks.
The impact ofcontainer size was examined in a second
set of experiments conducted in 200-mb finger bowls.
The experimental design was similar to the first except
that the treatments with six Daphnia and three Simo
cephalus and the individual species with Hydra were
eliminated. All treatments were run in triplicate. Again,
all individuals in each finger bowl were enumerated
weekly during the seven week duration of the experi
ment.
Data were analyzed using an analysis of variance
which took into account the experimental design of three
factors (experiment, species, and weeks) with repeated
measures on only one of the factors (weeks) (Winer,
1962). The large differences between initial and final
population size from each of the preceding experiments
necessitated the use of bog (x + 1) transformed data for
statistical analysis. The experiment initiated with twice
as many Daphnia as Simocephalus was not included in
this analysis.
A final competition experiment was conducted in 1001aquaria filled with 85 1of synthetic pond water. There
were two control and two treatment aquaria. All aquaria
were initiated with 20 individuals each of D. pulex and
S. vetulus. In addition, the experimental aquaria also re
ceived a single Hydra. The aquaria were checked at two
day intervals and maintained at 85 1with the same algal
mixture used in the other experiments. This experiment
was allowed to run for six weeks at which time the con
tents ofthe aquaria were filtered through a plankton net
and preserved in ethanol. Due to the large number of
individuals present in the aquaria at this time, the mdi
viduals from three subsamples were sorted to species,
counted, and then dried at 80°Cfor 24 h and weighed.
The remainder of each sample was then dried and
weighed in the same manner and the total number of
individuals belonging to each species estimated on the
basis ofits abundance in the original subsamples.
Results
The results of the small cup and finger bowl experi
ments were similar, differing primarily in their final pop
ulation size. The finger bowls supported about 50% more
individuals of both cbadoceran species (compare Figs. 1
and 4). The rapid numerical increase in all vessels mdi
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149
IMPACT OF PREDATION ON COMPETITION
160
140
C')
-J
0
>
0
z
120
I00
80
60
40
WEEKS
3
WEEKS
Figure 1. The mean population sizeofDaphnia pu/ex(circles)and
Simocephaius vetulus (squares) when grown separately in 100 ml cups
during a 5-week period. Bars represent ±2S.E.
Figure 2. The mean population size of Daphnia pulex (darkened
circles) and Simocephalus vetulus (darkened squares) when grown to
gether in 100 ml cups during a 5-week period. Open squares represent
cates the adequacy
of the feeding regime. Visual inspec
the mean total cladoceran population in the cups. Bars represent ±2
S.E.
tion ofthe untransformed data (Figs. 1, 2, 4, 5) suggested
that the growth of all test populations
could be divided
into two distinct phases. A period of rapid, linear, popu
lation growth was followed by a period during which the
populations leveled off, apparently having reached their
“¿carrying
capacity.―The initial phase lasted three weeks
in the cups and four weeks in the finger bowls.
The analysis ofvariance (Tables I, II) indicated that in
both sets ofexperiments there was a significant difference
between the population
size in the control and experi
mental vessels. This may be due to the fact that the tra
jectory of total population growth was slower in the ex
Table!
ANOVAfor the 100-micup set of experiments
perimental vessels (compare Figs. 1, 2 and 3, 4). How
ever, the combined carrying capacity in all of the
competition vessels was greater than the population in
the control vessels, which may indicate that the two spe
cies utilized slightly different food resources.
There was a significant difference in population size
between the species only in the bowls (Table II). Thus, in
the bowls at least, there were significantly
fewer Simo
cephalus than Daphnia in the experimental vessels than
Table!!
ANOVAfor
bowlexperimentsSourcedfSSMSFBetween
200-mifinger
Sourcedf55MSFBetween
cups91.49A
l**B(species)10.160.164.36AB10.050.051.47Error60.220.04Within
.061
.0628.9
(experiment)11
bowls102.93A
(experiments)I2.242.2460.980*B
(species)10.260.266.97*AB10.180.184.88Error70.260.04Within
bowls7720.79C(weeks)619.613.27400.94*0AC60.040.010.86BC60.940.1619.140*ABC60.000
cups5014.15C(weeks)511.942.3935.16**AC50.020.000.06BC50.060.010.20ABC50.
100.020.28Error302.040.07
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150
S. S. SCHWARTZ AND P. D. N. HEBERT
180
160
140
0)
-J
120
:@
a I00
>
a
z
80
60
40
20
I
4
23
WEEKS
5
three weeks. Simocephalus achieved almost 40% of the
densities observed in the control population in the cups
until the fifth week when Hydra, which had been unable
to reproduce due to the bow densities of suitable prey,
died. Simocephalus then rapidly increased to 76% of the
size of the control populations. Similarly, in the finger
bowls, Simocephalus reached 82% of densities in the
control by the end ofthe seventh week (Fig. 4).
Similar results were observed in the aquarium study
indicating that the outcome was robust over a range of
container size (Fig. 6). In the aquaria lacking predators,
Daphnia outnumbered Simocephalus individuals al
though the two aquaria differed in degree of dominance,
the ratio being 1.4: 1 in one aquarium and 7. 1:1 in the
other. By contrast, all Daphnia individuals were ebimi
nated in the aquaria with Hydra. Because only one Hy
dra was used to initiate the experiment, Daphnia popuba
tions expanded before the Hydra reproduced sufficiently
to make a significant impact on their density. However,
the large Daphnia population then served as food for the
rapidly
increasing
predator
population.
Bytheendofsix
weeks, all Daphnia individuals had been eliminated leav
Figure 3. The mean population size ofDaphnia pulex(circles) and
Simocephalusvetulus(squares)from an initial population containing
twice as many individuals of Daphnia as Simocephalus. The animals
were grown in lOO-mlcups for a 5-week period. Barsrepresent±2S.E.
200
180
in the control vessels. In both sets of experiments there
160
was a significant difference associated with time, i.e., not
surprisingly the populations were significantly larger at
the end ofthe observations than at the beginning.
The only interaction term found to be significant was
the species by vessel interaction in the bowl experiments,
i.e., the species were changing in a different manner
U)
-J
through time. Most likely the Daphnia
a
population
grew
faster in the experimental bowls than the Simocephalus
population through a suppression of the batter by either
exploitative or interference competition.
Competitive replacement did not occur in any of the
competition vessels, including the cups initiated with six
Daphnia and three Simocephalus (Fig. 3). After only two
weeks, Daphnia made up more than 90% ofthese popu
lations. By the end of five weeks, Simocephalus popula
tions had decreased to less than 5% ofthe Daphnia popu
lation. Dc Bernardi and Manca (1982) similarly found
that competitive replacement is a slow process with Si
mocephalus populations persisting at low densities over
a long period.
Those vessels which were initiated with Hydra in addi
tion to the cladocerans all showed the same pattern:
Daphnia individuals were eliminated in 97% ofthe yes
sels within the first week and, in all cases, by the end of
@I20
I00
@80
60
40
20
I
Figure 4.
234567
WEEKS
The mean population
size ofDaphnia
pu!ex(circles)
and
Simocephalusvetulus(squares)whengrown separatelyin 200-mi finger
bowls during a 7-week period. The mean population size ofS. vetulus
in the presence of Hydra is indicated by triangles. Bars represent ±2
SE.
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151
IMPACT OF PREDATION ON COMPETITION
limit the impact of predation. The cost of these adapta
tions is, in part, responsible for the differing competitive
ability ofthe two genera.
Simocephalus is a genus that occupies the littoral zone
where many of the predators employ ambush tactics
(Greene, 1985). Faced with such predators one success
ful prey strategy is to avoid ambush by not swimming.
Consequently, the sedentary behavior of Simocephalus
can be viewed as a means of avoiding predation. Simo
cephalus makes use of glands on the dorsal portion of
the carapace which allow it to attach to substrates and
continue filter feeding. This behavioral adaptation frees
Simocephalus ofcertain constraints on morphology; i.e.,
the cost of developing a more robust exoskeleton is de
rived solely from costs of producing the structure,
whereas planktonic cladocerans incur additional costs
associated with increased weight.
200
180
160
Cl)
-J 140
:@120
a
?l00
a
@80
60
40
Physiological
20
I
234567
WEEKS
Figure 5. The mean population size ofDaphnia pu!ex(circles) and
Simocephalusvetulus(squares)when grown togetherin 200-mi finger
bowls during a 7-week period. Open squares represent the total cladoc
eran population. Bars represent ±2SE.
adaptations
similar to that which allows
Simocephalus not to elicit the firing of coelenterate ne
matocysts have evolved many times in the Crustacea.
Cyprid larvae of the barnacle Ba/anus crenatus do not
elicit the discharge of nematocysts nor the mouth open
ing response of Obelia dichotoma (Standing, 1976) al
though larvae that are damaged are consumed. Numer
ous copepod genera live in association with sea anemo
nes (Gotto, 1979; Humes, 1982). A well-studied example
Daphnia
ing an average of 9625 Simocephalus and 853 Hydra.
There were many more Simocephalus in the experimen
tab aquaria than total cladocerans
Simocephalus
in the control aquaria.
Discussion
It has often been demonstrated that predators may de
termine the outcome of competition between two prey
species (Kerfoot, 1975, 1977; Jacobs, 1978; O'Brien
and Vinyard, 1978; Cooper and Smith, 1982). In the
present study the rapidity of the predators' effect de
pended on container size and was observed within a few
days or at most a few weeks. As observed in previous
studies, Daphnia outcompeted Simocephalus in the ab
sence of predators. This latter result is in part due to Si
mocepha/us reducing its reproductive rate in the pres
ence ofDaphnia, but ofgreater importance is the higher
intrinsic reproductive rate of Daphnia. However, in the
presence of predators the outcome of competition was
determined by the evolutionary interaction between Si
mocephalus and these predators. Daphnia and Simo
cephalus have faced different predation regimes over ev
obutionary time and have responded
to these differing se
bective pressures with unique suites of adaptations to
v)
4
>
6000
ID
w
4000
2000
0
Figure 6. A comparison of the cladoceran populations in 100-1
aquaria after 6 weeks. The two pairs of columns on the left represent
the two control aquaria and the other two pair represent aquaria to
which Hydra were also added.
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S. S. SCHWARTZ AND P. D. N. HEBERT
152
is Paranthessius anemoniae, which moves freely over the
tentacles ofAnemonia sulcata (Briggs, 1976). However,
free-living copepod species are paralyzed and consumed.
In addition, an extract ofthe anemone's tentacles caused
paralysis among the free-living copepods but not in P.
anemoniae. Similar results have been reported for the li
chomolgid cope@, Doridicola, which lives on a num
ber of species of anemones and does not elicit the firing
of nematocysts (Lonning and Vader, 1984). There are
also amphipods which are associated with sea anemones
that are immune to its host's toxins (Vader and Lonning,
1973).
The immunity to coelenterate nematocysts has also
been suggested to be important in determining the out
come of competition between two hermit crab genera,
Pagurus and Clibanarius
(Wright,
1973). The former ge
nus is able to occupy shells to which hydroids are at
tached, while the latter genus is stung and therefore can
not inhabit these shells. Thus the adaptations of Simo
cephalus are similar to those found in a number of other
crustaceans. A likely explanation is that Simocephalus
has evolved biochemical products that mask its presence,
as the first step in the firing of nematocysts by Hydra is
chemosensory (Lenhoff, 1968). Once this mask is
breached, Hydra readily consumes Simocephalus
(Schwartz et a!., 1983). The energetic cost ofsuch an ad
aptation
has not been determined,
but is most likely
small in comparison with the benefits.
In contrast to Simocephalus, Daphnia is unable to
evolve adaptations to predators that would compromise
its success in the open water environment. Behaviorally,
Daphnia actively avoids macrophytes (Pennak, 1973;
Dorgebo and Heykoop, 1985), which are obvious indica
tors of the littoral zone and the suite of predators that
lurk within. By avoiding the littoral zone Daphnia ne
gates the need for adaptations necessary to deter those
predators. In addition to being sensitive to Hydra preda
tion, Daphnia has been shown to be more easily captured
than Simocephalus by damseifly naiads (Akre and John
son, 1979; Johnson and Crowley, 1980) and the rhabdo
cod flatworm Mesostoma lingua (Schwartz and Hebert,
1986), most probably because it is constantly swimming
while Simocephalus is sedentary.
Members ofthe genus Daphnia have evolved a variety
ofmorphobogical adaptations whose function can be ex
plained as predator deterrence. In general, these adapta
tions consist of cuticular extensions to the head, tail
spine, and fornices, as opposed to cuticubar thickening
which would increase weight and lead to major increases
in basal metabolic rates. Morphological adaptations take
two forms—those that have evolved as permanent struc
tures and those that are produced in the presence of par
ticular predators. Dodson (1984) documented the costs
of the permanent adaptations of D. middendorffiana to
predation by the copepod Heterocope septentrionalis. He
suggested that these adaptations result in a lower repro
ductive rate of D. middendorfJlana compared to that of
its competitor, D. pulex. The cost to D. pulex is its elimi
nation from those habitats containing the copepod,
while D. middendorJJiana is limited to living with its
predator rather than its competitor.
The other class of morphological anti-predator adap
tations ofDaphnia are temporary features cued by chem
icals produced by particular predators, a phenomenon
recently termed chemomorphosis (Hebert and Grewe,
1985). Predators known to cause these effects are larvae
ofthe phantom midge Chaoborus(Krueger and Dodson,
198 1; Hebert and Grewe, 1985) and notonectids (Grant
and Bayly, 198 1; Barry and Bayly, 1985). The value of
these morphological alterations in reducing predation
has been demonstrated (Krueger and Dodson, 1982; Ha
vel and Dodson, 1985), but Dodson (1984) has shown
that even small cuticular extensions such as nachen
zahnen reduce the intrinisic rate of increase.
Daphnia and Simocephalus have faced unique sebec
tive pressures for adaptations deterring predation from
the predators they most frequently encounter. An impor
tant consequence of these adaptations involves the co
occurence ofthese cladocerans. The two species often co
occur in ponds that are large enough to support both lit
torab and pelagic zones (Anderson, 1974; pers. obs.).
Ponds backing either of these habitats are typically nu
merically dominated by one ofthe genera. Habitats lack
ing ambush predators (rock pools for example) are domi
nated by Daphnia as Simocephalus are excluded (Gan
ning, 197 1; Ranta, 1979), most probably by continued
competitive pressure. As observed in the aquaria study,
Simocephalus can produce considerable populations in
the absence of competitors but has smaller populations
when co-occurring with Daphnia. These reduced popu
lations may be due to both exploitative competition and
antagonism between the two genera. Inhibitory sub
stances have been proposed to be important in zooplank
ton species interactions (Frank, 1952; Seitz, 1984).
At the other habitat extreme, those ponds with a high
density of macrophytic growth and the associated inver
tebrate predators often back Daphnia but contain barge
populations of Simocephalus (pers. obs.). Species distri
bution is made more complex by the fact that Daphnia
becomes a browser when pbanktonic food resources are
limited (Mitchell and Williams, 1982). At such times
Daphnia is particularly vulnerable to littoral and benthic
predators. Therefore, the distribution of the two species
is regulated by a surface area:volume ratio that takes into
account not only morphometric contributions to surface
area but also that due to macrophytes.
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IMPACT OF PREDATION ON COMPETITION
In conclusion, we have demonstrated in laboratory ex
periments that the outcome of competition between
Daphnia and Simocephalus is regulated by the presence
ofHydra. The broad range ofmorphobogical and behav
ioral adaptations to predation place Simocephalus at a
competitive disadvantage. The divergence oflife history
characteristics
between
the species may be partially
a
product of competitive interactions. Daphnia, which
faces a different suite of predators, may have evolved a
unique assortment ofadaptations constrained by the ne
cessity ofmaintaining
itselfin the plankton.
Acknowledgments
This research was supported by a grant from the Natu
rab Sciences and Engineering Research Council to
P.D.N.H. Comments by anonymous reviewers im
proved this manuscript as well as the comments of G.
Cameron and L. Weider on early drafts. All are appreci
ated.
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