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Effects of large gut volume in gelatinous
zooplankton: ingestion rate, bolus
production and food patch utilization
by the jellyfish Sarsia tubulosa
LARS JOHAN HANSSON* AND THOMAS KIØRBOE
DANISH INSTITUTE FOR FISHERIES RESEARCH, KAVALERGÅRDEN 6, DK-2920 CHARLOTTENLUND, DENMARK
*CORRESPONDING AUTHOR: [email protected]
Received February 17, 2006; accepted in principle May 3, 2006; accepted for publication July 24, 2006; published online August 4, 2006
Communicating editor: K.J. Flynn
Many gelatinous zooplankton consume a large amount of prey and have stomach volumes much
greater than the volume of individual prey. We suggest that jellyfish can use their voluminous stomach
as a buffering food-accumulating organ that allows the organism to feed at maximum clearance rate
in a wide range of fluctuating food concentrations. The food accumulation capability was confirmed
for the hydromedusa Sarsia tubulosa feeding on copepods. Starved jellyfish feeding in high prey
concentrations for 1 h displayed much higher average ingestion rates compared with jellyfish feeding
for 20 h or with jellyfish that were pre-adjusted to the food concentration before incubation. The
findings have implications for design and interpretation of experiments. The possibility for jellyfish to
feed at maximum clearance rate in either very high prey concentration for a short time or low prey
concentration for a long time was illustrated with calculations of prey uptake by S. tubulosa feeding
in prey concentrations of variable heterogeneity. The ability of jellyfish to capture prey at maximum
clearance rate under different prey concentrations, and to accumulate relatively large amounts of food
in their guts, suggests that they would thrive in both homogenous and patchy food distributions. This
property may have contributed to the evolutionary and ecological success of the medusoid ‘bauplan’.
INTRODUCTION
Gelatinous zooplankton often display a high individual
predation potential. The animals are sometimes
regarded as organisms that constantly remove prey
from the sea water at maximum clearance rate.
However, experimentally determined ingestion rates (I )
are sometimes (e.g. Reeve and Walter, 1978; Sørnes and
Aksnes, 2004) far higher than that of jellyfish and ctenophore gut evacuation rates (D), which are typically less
than one prey per hour (Purcell, 1992; Martinussen and
Båmstedt, 1999; Purcell, 2003). A situation where I > D
is not in steady state but implies that over time prey will
accumulate in the predator. In high prey concentrations,
a high consumption rate therefore probably only applies
to short periods, whereas consumption rate over longer
time periods will be limited by digestion rate.
Ingestion rate estimates from short-time incubations
with starved predators always reflect the combined result
of ingestion rate and the ability of the predator to accumulate food in the stomach. Because the stomach in
many coelenterates is relatively large, it can take a long
time to fill it, and for reduced clearance rate to occur
‘fooling’ an investigator into thinking that a steady-state
ingestion rate has been attained when it has not.
One implication of such a prey-accumulating capacity by gelatinous zooplankton would be that they are
able to efficiently utilize a patchy food environment by
feeding at maximum rate in dense patches while
doi:10.1093/plankt/fbl030, 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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accumulating captured prey for the completion of digestion and assimilation when food availability is low. For
jellyfish and ctenophores, the effects of patchy prey
distributions have not previously been specifically
addressed.
A second implication is that incubation time must be
considered when experiments to estimate feeding rates
are designed and interpreted. A previously starved predator exposed to high prey concentrations will ingest
prey at an average rate that is dependent on the duration
of the incubation. Initially, it could feed at maximum
rate, but as gut space gets filled up, the instantaneous
feeding rate declines until it equals digestion rate. This
affects such kinetic calculations in all organisms; it is just
that in organisms with large guts, such as coelenterates,
the period of satiation may comprise a large part of the
total period of incubation.
In this study, we compare estimates of ingestion rates
in the hydromedusa Sarsia tubulosa derived from shortand long-term feeding sessions and examine the efficiency by which this species may utilize a patchy food
environment.
METHOD
Sarsia tubulosa captures prey with its four tentacles, and
prey are then transferred to the mouth and further into
the stomach where digestion occurs (Hernande and
Passano, 1967; Passano, 1973). For copepod prey,
transfer time is much shorter than digestion time
(Hansson and Kiørboe, 2006). Copepods are not completely digested by Sarsia, and the remaining chitin
skeletons are ejected in boluses (Fraser, 1969; Daan,
1986). Medusae of S. tubulosa, collected from
Limfjorden and Kertinge Nor (Denmark), were used
as predators in the experiments. Bell height was used
as size measure of the jellyfish. Three-week-old laboratory-reared Acartia tonsa were used as prey. All incubations were performed in the laboratory at 6–118C, i.e.
ambient sea water temperature for the area, in
darkness.
Effects of foraging time and pre-incubation
Jellyfish ingestion rate was measured from bottle incubations with a known number of predators (n = 1–5) and a
known initial prey concentration (C0). Bottles of defined
volumes (V = 305–2310 mL) were completely filled
with 0.2 mm of filtered sea water and sealed during the
incubations. Final prey concentration (Ct) was determined after each incubation from the number of remaining prey in the bottles. Controls without jellyfish were
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used to correct for handling errors. Individual ingestion
rate (I ) was calculated as:
V
ðC0 Ct Þ
I ¼
nt
where t is incubation time. I was plotted against the
geometric mean of prey concentration to describe the
functional response to prey concentration. Maximal
ingestion rate (Imax) was estimated by fitting a
Michaelis–Menten-type function to the data:
I ¼
Imax C
Kd þ C
where Kd is the prey concentration when I equals half
Imax.
Because we hypothesized that I would depend on t for
a jellyfish with an empty gut feeding at high prey concentration, we compared the functional responses from
two incubation series with t = 1 h and t = 20 h for
jellyfish that had been allowed to starve for 24 h before
incubation start. To obtain a functional response curve
with jellyfish in equilibrium between I and D, we made
one incubation series where the jellyfish had been preincubated at the food concentration of interest >3.5 h
before incubation, i.e. these jellyfish were allowed to
feed before the incubation measurements started. In
this case, I should be independent of t, which was set
to 24 h.
Food boluses and gut volume
As a measure of the gut accumulation capacity of
S. tubulosa, we counted the number of A. tonsa remains
in boluses produced by medusae feeding individually in
0.5-L tanks under ad libitum copepod concentration
(200 prey L–1). The tanks were inspected every day,
and any boluses were carefully removed from the
bottom of the tanks with a wide-mouth pipette
(Ø = 1 cm). Bolus size was measured with a microscope fitted with an ocular scale, and the number of
copepods in a bolus was estimated from counts of the
remaining chitin skeletons.
The gut contents of field-collected and preserved specimens of S. tubulosa (see Hansson and Kiørboe, 2006, for
sampling details) were dissected under microscope to
evaluate whether food in the stomach of actively feeding
jellyfish contains prey in different states of digestion (suggesting multitasking of prey capture and food digestion)
or whether prey were homogenously digested (suggesting
that the events of digestion and prey capture are separated in time).
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RESULTS
Effects of foraging time and pre-incubation
Figure 1 shows the functional response curves of S. tubulosa.
Ingestion rate (I ) of pre-incubated jellyfish increases with
food concentration to a plateau (Imax) where the gut is full
and cannot accept more prey until some food in the gut
has been digested or discarded. Thus, at the plateau, I is
limited by gut evacuation rate (D). Below the plateau concentration, I is instead limited by the prey capture rate (i.e.
the product of encounter rate and prey-handling efficiency). The functional response curve from pre-incubated
jellyfish represents long-term feeding of Sarsia in a constant
food environment. The shape of this functional response
curve strongly contrasts with that of short-term feeding
pre-starved Sarsia, where I increases nearly linearly with
prey concentration. This response curve shows the capacity of a starved jellyfish to feed at high rate in a dense
patch of prey, and the curve will reach Imax only when
maximum prey transfer (from capture tentacles to the
stomach) rate is reached. In another study, we estimated
the time for prey transfer as 0.11 h per prey (Hansson and
Kiørboe, 2006), which yields a maximum prey-processing
rate of 218 prey per day. This Imax for short-term feeding
1h
20 h
Equilibrated
–1
–1
Ingestion rate (copepods jellyfish d )
200
150
starved jellyfish is close to maximum observed I in Fig. 1.
As expected, the slopes of the functional response curves at
low prey concentrations, which represent maximum
clearance rates (Fmax), were relatively similar between
short-time incubations and incubations with equilibrated
predators. This is because at low prey concentrations, the
average time interval between successive ingestion events is
longer than gut evacuation time, and I is thus not limited
by D. Estimated Fmax-values for S. tubulosa were 0.98 and
2.5 L jellyfish–1 day–1 for 1- and 24-h incubations, respectively. The discrepancy may stem from how well the
ingestion curves fitted measured data points.
Food boluses and gut volume
Boluses were usually shaped as blunt-tipped cones and
contained the remains of several prey items held together
within a matrix of mucus (Fig. 2). Identifiable remains
from digested A. tonsa were the chitinous exoskeletons,
the red retina of the nauplius eyes, and copepod gut
remains. No undigested copepods were retrieved in discarded boluses. Sarsia tubulosa feeding on adult A. tonsa
discarded food boluses with varying number of copepods
(Fig. 3). The number of copepod remains is a relatively
good indicator of bolus size (Fig. 3A). A food bolus is
generally smaller than the sum volume of undigested live
copepods, but because mucus makes up a substantial
part of the bolus, the volume is not as different as when
the bolus was made up of only the exoskeletons and guts
of the ingested copepods. We once observed an individual Sarsia discarding a bolus with the effect that the
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0
0
100
200
300
400
Mean prey concentration (copepods L–1)
Fig. 1. Ingestion rate of Sarsia tubulosa feeding on 3-week-old Acartia
tonsa at 6–118C. Laboratory incubations lasted 1 h (black dots) or 20 h
(grey squares) using pre-starved jellyfish, or 24 h with jellyfish that had
been pre-incubated in the concentration of interest (white diamonds).
Slope of lines show maximum clearance rate for equilibrated jellyfish
(dashed line) and 1-h-incubated jellyfish (dotted line). There were not
adequate data at low prey concentrations to accurately estimate initial
slope of regression for 20-h-incubated jellyfish; 20 h data are from
Hansson et al. (Hansson et al., 2005) and 24 h data are from Hansson
and Kiørboe (Hansson and Kiørboe, 2006).
Fig. 2. Backlit photograph showing seven food boluses ejected by
Sarsia tubulosa feeding on Acartia tonsa copepods. Two dead copepods
are shown for size comparison (body length = 0.8 mm). The boluses
were ejected from the manubrium with the rounded tips of the boluses
first. Dark spots within the boluses are the contents of copepod guts and
nauplius eye retinas.
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B
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Copepods bolus
–1
40
0
0
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
2
3
4
10
12
Medusa height (mm)
Bolus volume (mm )
Fig. 3. The number of Acartia tonsa remains within boluses of Sarsia tubulosa feeding in high prey concentration. (A) The number of copepods per
bolus as a function of bolus volume. A linear regression was fitted to the data (black line, y = 23.7x + 0.34, r2 = 0.78). Dotted line illustrates the
number of non-digested copepods without mucus that would fit in a bolus (y = 37.7x). (B) Copepod content in boluses from seven differently sized
medusae. Linear regression fitted to the data (y = 0.58x + 3.4, r2 = 0.032), y is the number of copepods per bolus.
manubrium lost its bulging shape and became thin and
slender. This single observation indicates that all or most
of the gut contents are discarded when a bolus is ejected
and that bolus size therefore can be used as an approximation of gut accumulation capacity. However, if the
jellyfish does not evacuate all the gut contents simultaneously, our estimate of gut volume will be slightly conservative. The number of copepod remains per bolus,
which can be used as a measure of bolus size and indirectly gut volume, increased with jellyfish size (Fig. 3B).
Variation was high, but there was a size effect (median
number of copepods per bolus was higher in >8-mm
Sarsia than in <8-mm Sarsia; P = 0.026, Mann–
Whitney rank sum test). Individual jellyfish from
Limfjorden contained in their stomachs prey in different
stages of disintegration, suggesting that S. tubulosa simultaneously captures prey and digests food.
DISCUSSION
There was a clear effect of incubation time in the experiments with starved predators. The dependence of incubation time is evident when long-term incubations (20 h)
are compared with short-term incubations (1 h).
Accordingly, estimated Imax was highest for 1-h incubations, lower for 20-h incubations and lowest for jellyfish
that had been pre-incubated with prey for some time and
hence had a constant I/D-quotient (Imax was 520, 56, and
12 prey jellyfish–1 day–1, respectively). Similarly, the halfsaturation concentration—i.e. the prey concentration
where 0.5 Imax is reached—was highest for shortterm incubations, lower for long-term incubations and
lowest for equilibrated jellyfish (Kd was 530, 170, and 4.9
prey per litre, respectively). For a predator with voluminous stomach and I > D, we must thus consider that if
the predator was starved before the incubation, the predation rate estimate depends on incubation time. Only if
the predator has been pre-incubated, hence its gut preloaded so that it is in steady state with the experimental
prey concentration, will the shape of the functional
response curve be independent of incubation time. It is
noteworthy that maximum clearance rate can be estimated from the initial slope of the ingestion curve independently of incubation time (Fig. 1).
The digestive process of Sarsia has not been investigated
and remains enigmatic. Because feeding jellyfish from
Limfjorden contained a mix of prey in different stages of
digestion, the predators appear to ingest prey while digesting other prey, but discarded boluses only contained fully
digested prey. This suggests either that the jellyfish possess
some prey-sorting mechanism that retains non-digested
prey while a bolus is discarded or that the jellyfish actually
halts ingestion for some time before discarding a food
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P r e y in g u t , P t
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–1
bolus. The latter was not observed in mechanistic studies
of prey capture (Hansson and Kiørboe, 2006) in support
of the former hypothesis.
Ingestion rates estimated from short-term incubations
were high and hardly affected by digestion limitation,
demonstrating the capacity of jellyfish to take advantage
of high prey concentrations (such as extreme prey
patches) for short times. We may further characterize
the effect of prey accumulation capacity on the feeding
rate of a jellyfish in a patchy food environment by first
noting that the consumption rate of an individual jellyfish
may be limited by the rate that it encounters prey, by the
rate that prey is transferred from the tentacles to the
mouth, or by the digestion rate. The lowest of these
rates limits the long-term consumption rate. Which process is limiting for S. tubulosa depends on the patchiness of
the prey, the maximum transfer rate of prey from the
tentacle into the mouth (Tr = 9 prey per hour), the
maximum gut evacuation rate (D = 0.7 prey per hour),
the maximum clearance rate [Fmax = 2.1 L ind.–1 day–1,
all values for a 5-mm S. tubulosa feeding on 3-week-old
A. tonsa according to Hansson and Kiørboe (2006)] and on
the gut accumulation capacity (G = 6.3 prey, Fig. 3B). At
constant prey concentration (non-patchy environment),
prey consumption rate is limited by encounter rate at
prey concentrations C < D/Fmax, and by gut evacuation
rate at higher prey concentrations, i.e. prey consumption
rate is never limited by gut accumulation capacity or by
prey transfer rate.
In a patchy environment, however, consumption rate
becomes dependent on gut accumulation capacity.
Consider, for example, an extreme environment consisting of patches with prey concentrations high enough to
allow the jellyfish to encounter prey at maximum rate,
i.e. C > Imax/Fmax, and with no prey outside these patches.
Here, the gut accumulation capacity becomes limiting
when the duration of patch visits exceeds G/Tr = 0.7 h
(disregarding that digestion may occur while the gut is
being filled). If the jellyfish leaves the patch with a full
gut, then it may digest for G/D = 9 h before the gut is
empty and it needs to encounter a new patch to fully
utilize its digestion capacity. In an optimally ‘designed’
patchy environment, the jellyfish thus just need encounter
one patch every 9 h and stay there for 0.7 h, i.e. for 8%
of the total time (Fig. 4, scenario i). There is a direct
proportionality between the gut accumulation capacity
and (i) the time between patch visits (governed by distance
between patches for jellyfish with constant motility
pattern) and (ii) the time that the jellyfish can feed at
maximum clearance rate within the prey patch (governed
by the size of the patches).
However, a jellyfish in nature would never experience
such extreme fluctuations in prey concentrations, and we
P r e y c o n c e n t r a t io n ( L )
L. J. HANSSON AND T. KIØRBOE
80
60
40
20
0
i
0
ii
20
40
60
iii
80
100
120
140
Time (h)
Fig. 4. Example of varying food concentrations wherein a 5-mm Sarsia
tubulosa could be feeding on Acartia tonsa at maximum clearance rate.
Simulation conditions were prey transfer time = 0.11 h, digestion
time = 1.4 h prey–1, Fmax = 2.1 L day–1 (from Hansson and
Kiørboe, 2006), 0 < prey in gut < 6.3 (from Fig. 3B). Ingoing values
of time and prey concentration were chosen to illustrate three different
food situations: (i) no food available except for short times of extremely
high density; (ii) diurnally varying food concentration and (iii) homogenous food concentration at steady-state concentration. Panel A shows
the number of prey in the gut. Panel B shows the prey concentration
needed to fulfil the conditions.
therefore simulated a scenario with less drastic fluctuations. This is perhaps most easily done by calculating gut
content in Sarsia after each short feeding session in a
series of successive constant (but different) prey concentrations and adjusting the foraging time or prey concentration during each feeding session so that the jellyfish is
never starving (always > 0 prey in the gut) and never
contains more prey than estimated mean number of
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copepods retrieved in discarded food boluses (Fig. 3B).
Thus, after each foraging session at a constant food
concentration, the number of prey in the gut (P) was
calculated as:
Pt ¼ Pt1 þ t ðIt DÞ
where Pt is the number of prey in the gut after time
interval t, Pt-1 is the number of prey in gut before time
interval t, and It is ingestion rate calculated as:
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species are found. Some of these species may thus have
the ability to efficiently utilize much larger prey patches
with longer time between patch visits than in the example with Sarsia. The ability to maximize energy intake
under different food conditions could have contributed
to make the medusa body plan of jellyfish so evolutionary
and ecologically successful. The ecosystem effect of the
suggested high ingestion rate by gelatinous zooplankton
in dense prey patches would be to erode small–intermediate-scale prey patchiness.
It ¼ Fmax Ct
where Ct is the constant prey concentration during the
feeding session. We assume that prey are ingested and
disappear from the gut after a time equal to gut evacuation time and that the gut must never be filled more than
the average number of prey in a bolus (i.e. 6.3 prey
according to Fig. 3B).
Figure 4 shows 5 days of foraging at maximum clearance rate under varying food concentrations, where the
condition 0 < Pt < 6.3 is met. It illustrates how a 5-mm
S. tubulosa can forage successfully (i.e. at maximum clearance rate) under very different food distributions. Scenario
i illustrates extremely fluctuating food concentrations,
where the jellyfish encounters prey concentrations >103
copepods per litre for 46 min and fills the gut at a rate
equal to prey transfer rate. Between those feeding frenzies,
there is no prey in the water. Scenario ii simulates a
diurnal variation in prey concentration. In scenario iii,
prey concentration is totally homogenous over time and
I = D at all times. In all scenarios, the long-term average
prey concentration = D/Fmax = 8.2 prey per litre (or
higher in situation i ). The average number of prey in
field-collected Sarsia was within the range 0–6.3
(Hansson and Kiørboe, 2006), which indicates that in
nature this jellyfish feeds near Fmax. Note that calculations
of the relative time required within and outside prey
patches are insensitive to the estimated value of G. Thus,
the shapes of the curves in Fig. 4(B) remain the same
irrespective of our estimate of G, and only the absolute
time that the jellyfish has to spend in different food concentrations is affected by the value of G.
The large stomach in many jellyfish can thus act as a
buffer that prevents the predator from becoming immediately satiated upon exposure to high prey concentrations and permits continuous feeding at maximum
clearance rate. The presented example with S. tubulosa
illustrates how a jellyfish with a relatively small gut can
feed at maximum clearance rate under highly different
prey concentration scenarios. Jellyfish species with extremely large gut capacities can be found within the class
Scyphozoa, in which several common large jellyfish
ACKNOWLEDGEMENTS
This study formed part of the project EUROGEL,
supported by the European Commission through
Contract No. EVK3-CT-2002-00074. We thank
Limfjordsamterne and L. Friis Møller for assistance in
collecting jellyfish.
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