Download Top-down impact by copepods on ciliate numbers and persistence

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Top-down impact by copepods on ciliate
numbers and persistence depends on
copepod and ciliate species composition
INGRID GISMERVIK*
DEPARTMENT OF BIOLOGY, UNIVERSITY OF OSLO, PO BOX 1066, BLINDERN, 0316 OSLO, NORWAY
*CORRESPONDING AUTHOR: [email protected]
Received September 9, 2005; accepted in principle December 12, 2005; accepted for publication February 3, 2006; published online February 9, 2006
Communicating editor: K.J. Flynn
Experiments with the copepods Acartia clausi, Centropages hamatus and Pseudocalanus sp. were
performed to assess the species-specific effect of these copepods on the development of monospecific
algae (Nephroselmis pyriformis) and ciliate communities (Strombidium vestitum, Strombidium
conicum, Strombidium sp. and Lohmanniella oviformis). It was hypothesized that potentially
switching copepods like A. clausi will stabilize the algal community by switching between ciliate
and algal food, in contrast to copepods with stereotypic filter feeding behaviour (Pseudocalanus sp.).
In treatments with Pseudocalanus sp. and C. hamatus, all ciliate species were wiped out in 2 days,
resulting in blooms of N. pyriformis. In treatments with A. clausi, two of the ciliate species were able
to persist, but the combined ciliate and copepod community was not able to control the algal bloom.
Ciliates became abundant in control treatments without copepods, but only S. vestitum and S.
conicum seemed able to establish grazing control. Hence, when evaluating the role of ciliates in food
webs, their actual numbers and species composition should be taken into account. Likewise, the
species composition of copepods may be crucial; these experiments demonstrate that small filter feeding
copepods may have tremendous impact on ciliate numbers.
INTRODUCTION
Copepods are identified as key species in the marine
pelagial, not only in the capacity of being a link between
primary producers and fish but as predators on other
consumers. For instance, through predation on ciliated
protozoa, they structure the marine food web by removing grazers with higher growth rates and specific grazing
rates (Gismervik et al., 1996; Stibor et al., 2004; Vadstein
et al., 2004). Copepods and ciliates may have overlapping
food spectrum, although ciliates operate in the lower end
of the size scale (grazing prey of 3–7 mm for the most
common naked ciliates), while small copepods of the
genera Acartia, Pseudocalanus and Eurytemora are more efficient in the size range of 15–40 mm (Gismervik et al.,
1996). Although copepods select larger food, they are
capable of feeding on small food items and proliferate
when food abundance is high (Stoecker and Egloff, 1987;
Støttrup and Jensen, 1990; Gismervik et al., 1996;
Nejstgaard et al., 1997; Broglio et al., 2004). Thus, they
engage in a relationship where they prey on their competitors, a feature termed intraguild predation (Polis and
Holt, 1992). Such trophic triangles are common in most
food webs, but ubiquitous in microbial webs, because of
the high plasticity in prey : predator size, as well as the
different feeding modes found among protozoa (Stoecker
and Evans, 1985; Strom and Loukos, 1998). When the
competitors differ substantially in terms of functional or
numerical response, removal of the most efficient predator has considerable impact on the common resource.
While ciliate growth rates are comparable to those of the
phytoplankton community, the metazoan community
has a considerable time lag in its numerical response
(Gismervik et al., 1996). Hence, a zooplankton community
consisting of ciliates would be able to respond numerically
to an algal bloom, while a copepod-dominated community could only respond by increasing their grazing
rates. A two-level system with fast-growing algae and
ciliates is not stable and could result in ciliates eliminating their food source. However, a simple system including copepods may potentially be stable, depending on
the species characteristics of the ciliates and copepods as
well as on the nutritional state of the system (Gismervik
doi:10.1093/plankt/fbi135, available online at www.plankt.oxfordjournals.org
Ó The Author 2006. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
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and Andersen, 1997). Identification of key organisms
and their function in the marine pelagial has now
become an issue in marine science (Bathman et al.,
2001), and one group that has attracted interest is
switching predators. It has been proposed that switching copepods, for example copepods that increase their
clearance rate when the concentration of an alternative
prey increases, should be able to control ciliate abundance in a way that ensures stability of the community
over a range of nutrient loads (Gismervik and Andersen,
1997). On the other hand, non-switching copepods will
sustain a high predation pressure on ciliates even at low
densities and thereby drive ciliates to extinction when
resources are increased. Some common pelagic copepods like Acartia display two different feeding modes,
either filter or ambush feeding ( Jonsson and Tiselius,
1990), and may thus switch from algal food to ciliate
food when ciliates respond numerically to increased
food levels. Other copepod genera, such as Temora,
Para- and Pseudocalanus, seem to devote most of their
time to filter feeding (Tiselius and Jonsson, 1990; van
Duren and Videler, 1995), and clearance rates do not
decrease at low food concentration as is the case for
Acartia (Paffenhöfer, 1988; Kiørboe et al., 1996;
Gismervik and Andersen, 1997). The ability to pursue
a jumping/escaping prey differs between these two
categories; while Temora sp. does not respond to an
escaping ciliate ( Jakobsen, 2002), Acartia sp. will reorient its body towards the prey and attack ( Jonsson and
Tiselius, 1990; Broglio et al., 2001). Between these feeding strategies falls the strategy of Centropages, a fast cruising copepod which also spends time suspension feeding
and jumping. The outcome of the predator–prey interaction also depends on the features of the prey: swimming behaviour, speed and jumping, as well as size and
palatability. The ability of some ciliates (Myrionecta rubra,
Halteria sp. and Strobilidium spiralis) to perform rapid
jumps decreases the probability of capture (Jonsson
and Tiselius, 1990; Wiackowski et al., 1994; Wickham,
1995; Broglio et al., 2001).
Experiments with the copepods Acartia clausi,
Centropages hamatus and Pseudocalanus sp. were performed
to assess the species-specific effect of these copepods on
the development of monospecific algal and ciliate communities. Four different ciliates of variable size were
used, whereof two were mixotrophs and two were
heterotrophs.
METHOD
Ciliates, copepods and water for the experiments were
collected from the outer Oslofjord, Norway, in May 2003
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(Strombidium vestitum experiment) and March 2004 (other
experiments). Ciliates were isolated and kept in nonaxenic monocultures in IMR/2 (Eppley et al., 1967)
growth medium at salinity 25, in dim light (24 mmole
m–2 s–1) in a 12 h light : 12 dark cycle. The prasinophyceae Nephroselmis pyriformis was used for food. The diameter of the flagellate was in the range of 4.5–5 mm
(based on CASY and Coulter counter measurements)
and the biomass was 10.1 ± 0.0005 pg C cell–1
(Gismervik, 2005). Ciliates were identified from protargolstained samples (Montagnes and Lynn, 1993): S. vestitum,
Strombidium conicum (Agatha and Riedel-Lorjé, 1997) and
Lohmanniella oviformis (Lynn and Montagnes, 1988), while
one of the species has not been described by modern
methods and was termed Strombidium sp. [see Gismervik
(Gismervik, 2005) for details on this species]. The latter
species was heterotrophic in contrast to the other two
Strombidiids that were mixotrophic. Length and volume
of the ciliates are given in Table I.
I used 1-L Duran glass bottles with 900 mL GF/Cfiltered seawater, autoclaved at decreased pressure and
time (5 min, 1058C) and added EDTA (final concentration 10 mM) for the experiments. Food algae and ciliates
were gently transferred from stock cultures by a pipette to
the experimental bottles. Start concentrations of N. pyriformis were in the range of 11 000–15 000 cells mL–1, except
for the experiments with Strombidium sp. without copepods,
where concentrations were higher (19 500 mL–1).
Copepods were collected by a WP/2 net with a closed
cod-end. Female copepods were picked individually,
rinsed and added to the bottles at concentrations of
10 (A. clausi), 8 (Pseudocalanus sp.) or 5 (C. hamatus) per 900
mL. There were three replicates for each treatment with
two exceptions; in the experiment with S. vestitum, there
were five replicates, and as one of the replicates was lost
during the experiment with Acartia sp. and S. conicum, only
two time series are given for this latter treatment. The
bottles were kept stationary in a 12 h light : 12 h dark cycle
(167 mmole m–2 s–1). No mixing was performed except
during sampling once a day, when 90 mL was withdrawn
after gentle mixing. The sample was used for ciliate and
Table I: Size of ciliates used in experiments
Ciliate volume (mm–3)
Species
Ciliate length (mm)
Strombidium vestitum
23 ± 2.9
6375 ± 2559
Strombidium conicum
48 ± 6.1
29 758 ± 10 393
Strombidium sp.
40 ± 3.4
22 082 ± 7198
Lohmanniella oviformis
18 ± 1.9
2952 ± 959
Measurements (mean ± SD) are taken from Gismervik (Gismervik, 2005);
volumes are estimated from microscopically measured cell sizes using
simple geometrical formulas.
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algal counts. After sampling, the experimental bottles were
added 90 mL fresh filtered water with nutrients (stock
solution of KNO3 and KH2PO4), resulting in a final rate
of 1 mM N day–1 and 0.1 mM P day–1. The experiment
lasted for 8 days, with daily sampling and 10% daily
renewal of water. The bottles were inspected for dead
copepods when sampled. Survival was good, but on a
few occasions, dead copepods were found, and these
were replaced with living animals. At the end of the experiment, the content of the bottles was retrieved on a 35-mm
sieve. All copepods ±1 were found in all bottles, with the
exception of two bottles, in which three and four were
missing. Numbers of fecal pellets, eggs and nauplies were
enumerated from these samples. In addition to bottles with
copepods, two separate series of bottles with algae only and
algae and ciliates were included. These bottles otherwise
received the same treatment as the copepod bottles.
Ciliates from the experiments were fixed in 2% acid
Lugol’s and counted under an inverted microscope in
Utermöhl chambers. Algae were counted live by a
Coulter counter or by Lugol-fixed samples in a microscope or CASY Counter. Copepod carbon values used to
compare specific community grazing in treatments with
Acartia sp. and Pseudocalanus sp. were calculated from prosome length (L), which was converted to carbon weight
(W ) by a common regression of W = aLb, where a = 11.8
(95% CL of 9.8 and 13.7) and b = 3.1 (95% CL of 2.1 and
4.1) established by Gismervik et al. (Gismervik et al., 2002).
Copepod and ciliate clearance rates were calculated at
the start of the experiment, when clearance rates on
algae were supposed to be at maximum. Start samples
were withdrawn from the bottles after 1 h on day 0, and
stop values were obtained after 24 h. Growth rates of
algae and ciliates, and clearance rates for ciliates (F cil),
were calculated using start and stop values from bottles
containing algae only or algae and ciliates. As treatments
with copepods also included ciliates, ciliate grazing in
these bottles had to be taken into account. Clearance
rates for copepods feeding on algae (F cop) were calculated as F cop = F (cop + cil) – F (cil). F (cop + cil) was
obtained from treatments including copepods and ciliates. F (cil) was obtained from treatments with ciliates
and algae only and corrected for decline in ciliate numbers in copepod treatments by using the average ciliate
concentration of [C] = ([Ct] – [C0])(ln([Ct]/[C0])–1, where
[C0] and [Ct] are start and stop concentrations of ciliates,
respectively. Growth and clearance rates were calculated
in accordance with Frost (Frost, 1972). In the experiment
with A. clausi feeding on S. vestitum, samples were not
taken on day 0; hence, clearance rates were calculated
for day 1 till day 2. Ciliates were not sampled at day 2 in
the experiment with C. hamatus; hence, no feeding rates
were obtained for this species.
RESULTS
All copepod species had a severe impact on the ciliate
community (Fig. 1A–D). While ciliates proliferated in the
absence of copepods (Fig. 2), ciliates were decreased (Fig. 1A
and B) or driven to extinction in copepod bottles (Fig. 1C
and D). In treatments with A. clausi, S. vestitum were able to
uphold a small but stable abundance (Fig. 1A), and the
same was the case for one of the replicates containing
S. conicum (Fig. 1B). In contrast, Pseudocalanus sp. drove to
extinction all ciliate species in a matter of 2 days (Fig. 1B–D),
as did C. hamatus preying on S. vestitum (Fig. 1A). In the
treatment with L. oviformis, copepod bottles were added a
new batch of ciliates (final concentration 7 mL–1) at
day 5. Even though the algal numbers were very high at
this point (100 000–170 000 N. pyriformis mL–1) (Fig. 1H),
ciliate numbers were immediately decreased; in most
bottles, there were <1 ciliate mL–1 left after 24 h (Fig. 1D).
Nephroselmis pyriformis bloomed in all bottles with copepods, but moderately in treatments with A. clausi and
C. hamatus, compared to the treatments with
Pseudocalanus sp. (Fig. 1E–H).
To assess the well being of the ciliates, separate treatments with ciliates and algae only were performed. All
ciliates, except Strombidium sp., grew well and reached
high numbers by day 5 (Fig. 2). Strombidium sp. increased
the first days; thus the decrease in copepod bottles during
the first 2 days can be assigned to copepod predation,
rather than ‘natural’ death of ciliates, which appeared
after day 5 (Fig. 2C). Strombidium vestitum was the only
species able to graze down the food algae during the
8 days (Fig. 2A). Owing to rapid growth rates, they established dense populations within few days. Strombidium
conicum also seemed to establish some grazing control late
in the experiment; by day 6, numbers of algae started to
decline as ciliate numbers passed 30 mL–1 (Fig. 2B).
Average number of ciliates in copepod treatments was
calculated from day 1 till day 8 (Fig. 3), thus after the
initial decline in ciliate numbers (Fig. 1). Ciliate abundance was always higher in bottles with A. clausi compared to bottles with Pseudocalanus sp. and C. hamatus
(Fig. 3), although significantly so only for the treatment
with S. vestitum (t-test, log-transformed values, P = 0.0009).
Note that a new batch of ciliates was introduced at day 5
in the L. oviformis treatment, giving a high mean value for
this species (Fig. 3). Average ciliate numbers were lower
for all copepod treatments compared to bottles in which
ciliates were left without predators (Fig. 3).
Clearance rates on N. pyriformis measured in the beginning of the experiment did not differ much between
Pseudocalanus sp. and A. clausi in either experiment; values
were in the range of 5–22 mL copepods–1 day–1 (except
for one negative value obtained for Pseudocalanus sp.)
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Strombidium vestitum
400 000
A
–1
Acartia
Centropages
N. pyriformis mL
10
Ciliates mL
–1
8
6
4
2
E
Acartia
Centropages
300 000
200 000
100 000
0
0
Strombidium conicum
400 000
B
Ciliates mL
–1
8
–1
Acartia
Pseudocalanus
N. pyriformis mL
10
6
4
2
F
Acartia
Pseudocalanus
300 000
200 000
100 000
0
0
Strombidium sp.
10
400 000
C
N. pyriformis mL
–1
Ciliates mL
–1
Acartia
Pseudocalanus
8
6
4
2
G
Acartia
Pseudocalanus
300 000
200 000
100 000
0
0
Lohmanniella oviformis
400 000
10
–1
8
N. pyriformis mL
Acartia
Pseudocalanus
–1
Ciliates mL
H
D
6
4
2
Acartia
Pseudocalanus
300 000
200 000
100 000
0
0
0
1
2
3
4
5
Days
6
7
8
9
0
1
2
3
4
5
Days
6
7
8
9
Fig. 1. Abundance of ciliates (number mL–1) and Nephroselmis pyriformis (number mL–1) in treatments with different copepod species. (A) and (E)
Strombidium vestitum, (B) and (F) Strombidium conicum, (C) and (G) Strombidium sp. and (D) and (H) Lohmanniella oviformis.
(Table II). The numbers of copepods were kept higher in
treatments with A. clausi (10 copepods as opposed to eight
Pseudocalanus sp. per bottle) to ensure a total biomass of
50 mg C L–1 (estimated total biomass was 51 and 46 mg
C L–1 for A. clausi and Pseudocalanus sp., respectively).
Hence, the specific community clearance rates (at
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I. GISMERVIK
1000
600
A Strombidium vestitum
120000
300
60000
200
40000
70
120000
0.01
60
Lo Ps
50
–1
100000
60000
30
40000
20
20000
10
C i li ates mL
40
80000
70
C Strombidium sp.
Ps
Ac
S. conicum
Sp
Ps
Ac
Strombidium sp.
Sv
Ce Ac
S. vestitum
60
40
80000
60000
30
40000
20
20000
10
0
Ciliate clearance rates on N. pyriformis at the beginning
of the experiments were 0.01 mL ciliate day–1 for the
small species and 0.16 mL ciliate day–1 for the large
S. conicum (Table II).
–1
50
100000
Ci li at es mL
120000
Sc
Fig. 3. Average abundance of ciliates from day 1 to day 8 (mean ± SD)
in treatments with Nephroselmis pyriformis and ciliates (dotted bar), N.
pyriformis, ciliates and copepods (shades of grey). Note that the initially
high ciliate abundances are omitted from the calculated average abundance (day 0 not included). Note logarithmic scale. Ps, Pseudocalanus sp.;
Ac, Acartia clausi.
0
140000
Ac
L. oviformis
0
300000
DISCUSSION
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D Lohmanniella oviformis
250000
60
50
200000
40
150000
30
100000
20
50000
–1
–1
N. p yri fo rmi s mL
B Strombidium conicum
0
–1
1
0.1
0
140000
N. pyrif o rmis mL
10
100
20000
0
–1
Ciliates mL –1
400
80000
C i li ates mL
–1
100000
N . p yri f ormi s mL
100
500
Ci l iat es mL
–1
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Nephroselmis
Ciliates
140000
N . pyri f ormis mL
j
10
0
0
0
1
2
3
4
5
Days
6
7
8
9
Fig. 2. Concentrations of Nephroselmis pyriformis (number mL–1, primary axis) and ciliates (number mL–1, secondary axis) in treatments
without copepods; (A) Strombidium vestitum, (B) Strombidium conicum, (C)
Strombidium sp. and (D) Lohmanniella oviformis. Note different scale.
average food levels of 150 mg algal C L–1) can be
compared directly; these were in the range of 81–207
mL day–1 for A. clausi and 94–216 mL day–1 for
Pseudocalanus sp.
Clearance rates on ciliates in the beginning of the
experiment were considerably higher for Pseudocalanus
sp. than for A. clausi for all ciliates (Table II), but the
difference was only significant for S. conicum (t-test, logtransformed values, P = 0.02). Specific community clearance rates (at average food levels of 1.5–10 mg ciliate C L–1)
were in the range of 418–1879 mL day–1 for A. clausi and
1512–3060 mL day–1 for Pseudocalanus sp.
A number of experiments were performed in this study to
assess the species-specific impact of copepods on ciliates
and on a monospecific algal community. Three major
points can be made. First, copepod impact on ciliates
seems to be species dependent. Although the data were
scattered, the consistency among the experiments (ciliate
numbers were always higher in treatments with A. clausi
as opposed to treatments with Pseudocalanus sp.) suggests
that these two copepods have different impact on the
ciliate community. Second, the impact also depended on
the ciliate species present; while S. vestitum was able to
persist in treatments with A. clausi, other species were
removed immediately (L. oviformis). Third, the impact of
ciliates on the development of the algal bloom was species dependent; ciliate control relied on very high numbers of small ciliates (S. vestitum) or moderately high
numbers of larger ciliates (S. conicum), both resulting in
high population grazing rates.
Copepod feeding behaviour has attracted attention for
decades (Lowndes, 1935; Anraku and Omori, 1963;
Jonsson and Tiselius, 1990), and effort has been made to
categorize copepods according to different feeding strategies depending on morphological characteristics (Schnack,
1982; Landry and Fagerness, 1988; Paffenhöfer, 1998) as
well as swimming behaviour (Green, 1988; Tiselius and
Jonsson, 1990). This has led to theories suggesting how
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Table II: Clearance rates for ciliates feeding on Nephroselmis pyriformis and copepods feeding
on N. pyriformis and ciliates at the beginning of the experiment
Experiment
Ciliates (mL individuals–1 day–1)
Acartia (mL individuals–1 day–1)
Pseudocalanus sp. (mL individuals–1 day–1)
Algal food
Algal food
Ciliate food
Algal food
Ciliate food
Lohmanniella oviformis
0.01 ± 0.007 (2)
10 ± 4 (3)
197 ± 29 (3)
14 ± 9 (3)
425 ± 185 (3)
Strombidium sp.
0.05 ± 0.015 (3)
12 ± 2 (3)
261 ± 167 (3)
22 ± 6 (3)
402 ± 27 (3)
Strombidium conicum
0.16 ± 0.007 (3)
17 ± 0.1 (2)
62 ± 10 (2)
Negative
210 ± 75 (3)
Strombidium vestitum
0.01 ± 0.002 (5)
5 ± 5 (5)
58 ± 18 (5)
Values are expressed as mean ± SD (n).
various copepods will exploit different components of the
food web, for instance algae versus ciliates, small or nonmoving prey versus swimming/jumping prey (Kiørboe
et al., 1996; Broglio et al., 2001; Jakobsen, 2002, 2005).
The conclusion that copepods behave differently according to which prey is dominating further suggests that food
web stability and persistence depends on species composition. Copepod feeding strategies are commonly divided
into the categories filter feeders (Calanus, Pseudocalanus,
Paracalanus and Temora), ambush feeders (Acartia) or cruising/
filter feeders (Centropages). Although the categorization may
be correct, the conclusions regarding food intake that
are drawn may be wrong. A common perception has
been that filter feeders are typically algivores (feeding on
small and non/slow-moving prey), hence the generalization that these copepods are not capable of/efficient at
eating other prey. However, this study, as well as others
(Fessenden and Cowles, 1994; Nejstgaard et al., 1997;
Jakobsen et al., 2005), shows that these species are also
able to exploit larger moving prey like ciliates. Indeed, the
filter feeder in this study (Pseudocalanus sp.) wiped out ciliates
faster than the combined ambush–filter feeder (A. clausi). As
suggested in the Introduction, the stereotypic feeding of
Pseudocalanus sp. (a non-switching copepod) led to the
extinction of ciliates, as they do not decrease their clearance
rates at low food concentrations. The cruising predator
Centropages typicus feeds selectively on ciliates (Wiadnyana
and Rassoulzadegan, 1989), and in this study, its relative,
C. hamatus, efficiently reduced the numbers of S. vestitum.
Thus, both filter feeding and cruising copepods may have
tremendous impact on the ciliate community.
The outcome of the predator–prey encounter is a
result of several factors. An ambush copepod reacts to
hydromechanical signals from a swimming ciliate and
attacks (Tiselius and Jonsson, 1990). The ciliate detects
the copepod and may escape if its jumping/swimming
speed is fast enough (Jonsson and Tiselius, 1990; Broglio
et al., 2001). Hence, different ciliate species have different
vulnerability to copepod predators, according to their
behaviour (Wiackowski et al., 1994). As opposed to swimming, filter feeding copepods, a slowly sinking ambush
predator, has the advantage of not being detected until it
attacks. Thus, if Acartia sp. switches from ambush feeding
mode to filter feeding when ciliate abundance decreases
and algal abundance increases (as in this study), the
vulnerability of the ciliates will decrease. A filter feeding
copepod will trap a ciliate in its feeding current, given
that the currents velocity is greater than the escape
velocity of the ciliate ( Jakobsen et al., 2005). In this
study, all ciliate species seemed to be trapped in the
current generated by Pseudocalanus sp., as all were cleared
at high rates. However, Pseudocalanus sp. had a considerably higher clearance rate for L. oviformis and Strombidium
sp. than for S. conicum (Table II). As none of the examined
ciliates displayed jumping or other escape responses
(visual examination of cultures) in this study, the different
clearance rate observed must have been related to other
factors. Despite the differences in size, both the small L.
oviformis and the larger Strombidium sp. were cleared at the
same rate by Pseudocalanus sp. On the other hand, clearance rates on the almost similar sized S. conicum and
Strombidium sp. were quite different (Table II). Thus,
size seemed not to be the key point for this copepod.
The same pattern emerged for A. clausi—high clearance
rates on the two heterotrophic species, while the clearance rates observed for the two mixotrophic species were
considerably lower (roughly 25% of the rates obtained
for the heterotrophic ciliates). Hence, the differences in
feeding effort may have been related to the nutritional
status of the ciliates, as previously noted by Pérez et al.
(Pérez et al., 1997). In their study, heterotrophic species
seemed to be cleared at higher rates than mixotrophic
species. This conforms to the results of this study, with
rates in the range of 261–425 and 58–210 mL copepods–
1
day–1 for the heterotrophic and mixotrophic ciliates,
respectively.
Predator–prey interactions are also affected by external
factors like turbulence (Saiz and Kiørboe, 1995). In this
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Table III: Numbers of fecal pellets, eggs and
nauplies per copepod recorded by the end of the
study (mean ± SD)
Prey
Strombidium
Strombidium
Lohmanniella
conicum
sp.
oviformis
Fecal pellets
Acartia clausi
Pseudocalanus sp.
8±2
27 ± 12
5±4
204 ± 76
300 ± 27
79 ± 20
22 ± 11
9 ± 22
10 ± 14
Eggs
Acartia clausi
Nauplies
Acartia clausi
Pseudocalanus sp.
8±3
11 ± 5
4±1
19 ± 4
27 ± 8
14 ± 1
study, experimental bottles were not rotated or stirred;
thus, mixing only occurred during sampling once a day.
This may have influenced the feeding rate of A. clausi, as
feeding rate in ambush mode of this species may be
enhanced at certain levels of turbulence (Saiz and
Kiørboe, 1995). However, the point of this study was to
look for interactions among copepods and swimming prey,
and in that context, I found it important to keep the
experiment simple, with as few interacting factors as possible. Both algae and ciliates were active swimmers and
were distributed in the whole volume of the bottles.
Swimming N. pyriformis was initially evenly distributed in
the bottles, but in treatments with A. clausi, aggregates were
found after some days. The aggregation of algae late in the
experiment should not affect the conclusions in this study,
as the outcome of the copepod–ciliate interactions was
established earlier on. Furthermore, algal food levels
offered to the copepods were still high and dominated by
free-swimming cells. It is however of interest that the algal
bloom was considerably lower in all treatments with A.
clausi, as opposed to treatments with Pseudocalanus sp.; all
the time this cannot be explained by higher community
grazing rates by A. clausi or by the ciliates (the number of
ciliates left was too low to make an impact). Fecal pellets,
eggs and nauplies were recorded by the end of the study
and showed that all copepod species were able to proliferate on the food algae and ciliates (Table III). According to
these stop samples, Pseudocalanus sp. seemed to produce
considerably more fecal pellets and nauplies than A. clausi.
However, it should be taken into account that these numbers are subject to species-specific differences in pellet
breakdown, cophrophagy and cannibalism during the
8-day study.
One of the hypotheses in this article was that switching
copepods would tend to stabilize a three-component
system through intraguild predation. Indication of
switching by A. clausi in treatments with S. vestitum was
found, as ciliate numbers were kept low and stable during this experiment, while algal biomass increased. It
seemed like A. clausi concentrated on algal food when
ciliates were below a certain level. The level was, however, quite variable in the different bottles (2–8 ciliates
mL–1), indicating intra-specific variation. Although A.
clausi seemed to reduce its feeding effort on some ciliates
at low abundances, this did not arrest the algal bloom
and stabilize the three-component system. This was due
to the low numbers of ciliates left in the bottles. With a
clearance rate of 0.01 mL ciliate–1 day–1, eight ciliates
mL–1 would be able to clear 8% of the volume per day.
However, because of their high growth rates, S. vestitum
was able to take control and graze down the algal bloom
when no copepods were present. Strombidium sp. displayed a moderate response when copepods were
omitted; this may have been because of inadequate conditions for this species, such as high water exchange or
overgrowth of algae. It is not uncommon to find that
some ciliates do not thrive when algal numbers become
too high in the laboratory. On the other hand, S. conicum
was able to control the algal bloom in treatments without
copepods. The latter species displayed a high grazing
rate of 0.16 mL ciliate–1 day–1 in this study. In a compilation of maximum clearance rates for oligo- and choreotrich ciliates, Gismervik (Gismervik, 2005) found a
median maximum clearance rate of 0.7 mL ng C–1 h–1.
In the beginning of the experiments in the present study,
specific clearance rates were 0.5 and 1.18 mL ng C–1 h–1
for Strombidium sp. and S. conicum, respectively (based on
numbers in Tables I and II and a conversion factor of
0.19 pg C mm–3). Hence, the rates obtained were reasonable and conformed well to other studies ( Jonsson, 1986;
Kivi and Setälä, 1995; Gismervik, 2005).
The concentrations of S. vestitum left in treatments with
A. clausi were in the range found in natural waters (Pierce
and Turner, 1992). Hence, a significant impact of ciliates
on the algal community would demand higher ciliate
numbers/more efficient ciliates or lower algal growth
rates. Indeed, higher ciliate numbers are found in transient situations (Dale and Dahl, 1987; Montagnes et al.,
1999) or when copepod abundances are low (e.g. springtime in temperate waters) (Smetacek, 1981), and nutrient
limitation will often slow down algal growth rates.
CONCLUSIONS
These experiments demonstrate species-specific interactions between copepods and ciliates. Some ciliate species
were able to persist in treatments with the ambush predator A. clausi, while the two other copepods wiped out
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JOURNAL OF PLANKTON RESEARCH
j
VOLUME
all ciliates in few days. The filter feeder Pseudocalanus sp.
turned out to feed efficiently on all ciliate species. This
finding demonstrates the danger of extrapolating our
misconception of filter feeders as ‘not interested or capable of eating ciliates’ when analysing food web interactions. Rather, such notions should be tested under
controlled conditions, as well as in the field.
Furthermore, although ciliates are efficient grazers and
have rapid growth rates, the species composition and
actual numbers of ciliates should be taken into account
when evaluating their role in food webs.
ACKNOWLEDGEMENTS
I thank S. Brubak for help with the protargol stains and
T. Andersen and E. Bagøien for reading earlier drafts of
the manuscript and the referees for valuable comments.
28
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