Annals of Botany Page 1 of 8

doi:10.1093/aob/mcp269, available online at www.aob.oxfordjournals.org

Trap closure and prey retention in Venus flytrap (Dionaea muscipula)

temporarily reduces photosynthesis and stimulates respiration
Andrej Pavlovic*, Viktor Demko and Jan Hudak
Department of Plant Physiology, Faculty of Natural Sciences, Comenius University in Bratislava, Mlynska dolina B2, 842 15,
Bratislava, Slovak Republic
Received: 10 August 2009 Returned for revision: 11 September 2009 Accepted: 5 October 2009

Key words: Action potential, carnivorous plant, cost/benefit model, chlorophyll fluorescence imaging, Dionaea
muscipula, photosynthetic rate, respiration rate, Venus flytrap.

IN T RO DU C T IO N
Carnivorous plants have fascinated scientists for centuries, and
the Venus flytrap (Dionaea muscipula) is one of the most spectacular due to the rapid movement of its trap. Charles Darwin was
also fascinated by the Venus flytrap and called it one of the most
wonderful plants in the world (Darwin, 1875). Closure of the
Venus flytrap is one of the fastest movements in the plant
kingdom. The plant produces a rosette of leaves, each divided
into two parts: the lower called the lamina and the upper the
trap. The trap consists of two lobes, which close together
forming an enclosed pocket. Juniper et al. (1989) described
the trap as consisting of three zones. The first has 1421 marginal teeth on each lobe, which interlock when the trap snaps.
The second zone is a peripheral narrow band bearing small
sessile glands, which secrete carbohydrates, presumably as a
prey attractant. The third zone, the largest, is the whole central
zone which is covered with digestive glands. Among these are
bristles known as trigger hairs, usually three to a lobe. When
an insect crawls along the ventral surfaces and bumps into the
three small trigger hairs, the trap snaps shut. Two touches of a
trigger hair activate the trap which snaps in a fraction of
* For correspondence. E-mail pavlovic@fns.uniba.sk

second at room temperature. However, at higher temperature

(3540 8C) only one stimulus is required for trap closure
(Brown and Sharp, 1910). Darwin suggested that an impulse
must travel rapidly to enable the rapid response observed. In
response to Darwins request, Burdon-Sanderson (1873) discovered that the impulse was electrical and resembled the signal of
animal nerve and muscle. There is no doubt that action potentials
play an indispensable role in rapid plant movements. The action
potentials in Dionaea have been extensively studied (e.g.
Burdon-Sanderson, 1873; Hodick and Sievers, 1986, 1988,
1989; Sibaoka, 1991; Krol et al., 2006; Volkov et al., 2008a).
An electrical stimulus closes the trap without mechanical stimulation of the trigger hair, and repeated application of a lower
voltage demonstrates the existence of electrical memory in
Dionaea (Volkov et al., 2007, 2008a, b, c, 2009). However,
the mechanism by which the trap shuts is poorly understood.
The most frequent explanations are acid-induced cell wall loosening (Williams and Bennett, 1982) and rapid loss of turgor
pressure (Batalin, 1877). Trap closure occurs via rapid changes
in the curvature of each lobe rather than movement of the leaf
as a whole. Recently Forterre et al. (2005) provided a comprehensive analysis of leaf geometry during closure of the trap.
The driving force in closure is most probably the elastic

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Background and Aims The carnivorous plant Venus flytrap (Dionaea muscipula) produces a rosette of leaves:
each leaf is divided into a lower part called the lamina and an upper part, the trap, with sensory trigger hairs on
the adaxial surface. The trap catches prey by very rapid closure, within a fraction of a second of the trigger hairs
being touched twice. Generation of action potentials plays an important role in closure. Because electrical signals
are involved in reduction of the photosynthetic rate in different plant species, we hypothesized that trap closure
and subsequent movement of prey in the trap will result in transient downregulation of photosynthesis, thus representing the energetic costs of carnivory associated with an active trapping mechanism, which has not been previously described.
Methods Traps were enclosed in a gas exchange cuvette and the trigger hairs irritated with thin wire, thus simulating insect capture and retention. Respiration rate was measured in darkness (RD). In the light, net photosynthetic rate (AN), stomatal conductance (gs) and intercellular CO2 concentration (ci) were measured, combined
with chlorophyll fluorescence imaging. Responses were monitored in the lamina and trap separately.
Key Results Irritation of trigger hairs resulted in decreased AN and increased RD, not only immediately after trap
closure but also during the subsequent period when prey retention was simulated in the closed trap. Stomatal
conductance remained stable, indicating no stomatal limitation of AN, so ci increased. At the same time, the effective quantum yield of photosystem II (FPSII) decreased transiently. The response was confined mainly to the
digestive zone of the trap and was not observed in the lamina. Stopping mechanical irritation resulted in recovery
of AN, RD and FPSII.
Conclusions We put forward the first experimental evidence for energetic demands and carbon costs during
insect trapping and retention in carnivorous plants, providing a new insight into the cost/benefit model of
carnivory.

Page 2 of 8

Pavlovic et al. Photosynthesis during trap closure in Venus flytrap

M AT E R IA L S A ND M E T HO DS
Plant culture and experiments

Twenty 3- or 4-year-old Dionaea muscipula J. Ellis plants

were grown under standard greenhouse conditions at a

maximum daily irradiance of 1000 mmol m22 s21 PAR

( photosynthetically active radiation), in a collection of carnivorous plants at the Department of Plant Physiology in
Bratislava, in well-drained peat moss in plastic pots irrigated
with distilled water. All experiments were performed on
healthy leaves. Because the diameter of the cuvette window
used in gas exchange measurements was 18 mm, the traps
used in our experiments did not exceed this size. The
laminae were longer than 50 mm, because the size of the
cuvette head gasket plates was 45 mm. Leaves were cut near
the base, without causing closure of traps, and the upper part
of the leaf (trap) and thin wire (diameter approx. 0.1 mm)
inside the needle from a syringe plugged with silicone
grease were sealed into a leaf cuvette (PLC6, PP-systems,
Hitchin, UK) which monitors the CO2 and H2O exchange.
The bases of laminae were submerged in distilled water in
Eppendorf tubes to prevent drying out. Movement of the
wire in the empty, closed cuvette had no effect on CO2 and
H2O exchange, confirming that the movements of thin wire
had no effect on the gas-tight seal. After stabilization of conditions (leaf temperature 24 + 1 8C, ambient CO2 concentration 380 mL L21, relative air humidity 60 65 %), the
trigger hairs of the trap were mechanically stimulated by
manipulation of the wire protruding outside the cuvette. The
wire was placed between the two trigger hairs inside the
open trap, so just a very short movement (5 mm) was sufficient
for trigger hair stimulation. Two of the six trigger hairs inside
the trap were gently touched until the trap snapped: this is the
snap phase of the experiment. In the subsequent prey
struggle phase of the experiment the trigger hairs were repeatedly stimulated mechanically for 5 min with the wire inside the
closed trap whilst it was enclosed in the cuvette. Both experiments were repeated on the lower part of the leaf (lamina),
by enclosing only the lamina in the cuvette, with the trap protruding outside. The mechanical irritation was performed on
the trap outside the cuvette, with the same wire. Both experiments were repeated under light as well as dark conditions.
The experiments were repeated ten times for each experimental set-up with the same results. Because the trap of the Venus
flytrap rapidly changes geometry after closure (Forterre et al.,
2005), we wanted to exclude the possibility that reduced
photosynthetic parameters are due to changes of light interception by traps. Therefore, we irritated only one trigger hair by
one touch. One stimulus generates one electrical potential
(Volkov et al., 2008a) and we expected that photosynthetic
parameters would decrease without trap closure (trap geometry
remained unchanged). This experiment was repeated ten times
with the same results.
Gas exchange measurements

Gas exchange was measured using an infrared gas analyser

with an automatic leaf cuvette (CIRAS-2 and PLC6;
PP-Systems, Hitchin, UK). The rates of net photosynthesis
(AN), stomatal conductance (gs) and intercellular CO2 concentration (ci) were measured at a saturating irradiance of
1000 mmol m22 s21 PAR, leaf temperature 24 + 1 8C,
ambient CO2 concentration 380 mL L21, relative air humidity
60 65 % and water vapour deficit 700 1000 Pa. The rate of
respiration (RD) was measured under the same conditions at

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energy accumulated due to the hydrostatic pressure differences

between the upper and lower layers of the lobes. The electrical
signals open the water pores between these layers to open and
the water transfers from the upper to the lower layer.
Aquaporins may play an important role in this process,
because aquaporin inhibitors (e.g. HgCl2) inhibit trap closure
and ion channel inhibitors (e.g. lanthanum) reduce the amplitude
of action potentials (Krol et al., 2006; Volkov et al., 2008b, c).
After rapid closure secures the prey, chemical and mechanical
stimuli from the struggling prey result in a slow closing
process during which the whole trap is sealed into a tight
pouch. Soft parts of insect bodies are broken down by
enzymes and the digestive products are absorbed (Schnell,
2002). In this way D. muscipula growing in nutrient-poor habitats obtains up to 75 % of its nitrogen from insects (Schulze
et al., 2001).
Action potentials occur in many plant species, including
rapid leaf movements in sensitive plants and, irrespective
of rapid leaf movements, electrical signals also trigger physiological processes in plants which are not carnivorous or sensitive (reviewed by Fromm and Lautner, 2007). It has been well
documented that electrical signals propagated in plants over
long, as well as short, distances reduce photosynthesis. Thus,
heat stimulation evokes electrical activity and decreases photosynthesis in adjacent leaves in different species (Koziolek
et al., 2003; Lautner et al., 2005; Hlavackova et al., 2006;
Kaiser et al., 2006). This convincing evidence for a link
between electrical signalling and photosynthesis in response
to abiotic stress suggests that trap closure in Dionaea and
the associated electrical signals will decrease photosynthesis.
However, physiological effects in carnivorous plants in
response to mechanical irritation have not been investigated.
We hypothesized that trap closure and subsequent movement
of prey in the trap (simulation of insect retention) will result
in transient downregulation of photosynthesis. Because the
rate of net photosynthesis (AN) is a function of dark respiration
(RD) as well as of gross photosynthesis (AG), we also measured
the rate of RD. Carbon dioxide fluxes were measured by gas
exchange, and these were combined with chlorophyll fluorescence imaging to measure effective quantum yield of photosystem II (FPSII). This parameter measures the proportion of
the light absorbed by chlorophylls associated with photosystem
II that is used in photochemistry. Under laboratory conditions it
can give a measure of the rate of linear electron transport and so
an indication of overall photosynthesis (Maxwell and Johnson,
2000). Because photosynthesis and respiration are principal
points in cost/benefit analysis of carnivorous plants (Ellison
and Gotelli, 2009), we discuss our results with regard to the
cost/benefit model of carnivory proposed by Givnish et al.
(1984). We extended the classical interpretation of the model
(carnivorous plants with constant low AN in traps) by direct
carbon costs associated with insect trapping and retention,
which has not been previously described.

Pavlovic et al.Photosynthesis during trap closure in Venus flytrap

Chlorophyll fluorescence imaging

Stimulation of trigger hairs and subsequent trap closure very

rapidly decreased the rate of net photosynthesis (AN) of traps
to nearly zero. Then AN started to recover, reaching the rate
before mechanical stimulation within 10 min. In contrast, no
inhibition of AN was observed in the laminae (Fig. 1A).
Rapid inhibition of AN in traps resulted in a transient increase
in the intercellular CO2 concentration (Fig. 1B). Stomatal conductance (gs) was not affected, either in the traps or in the
laminae, indicating the absence of stomatal movements
(Fig. 1C). There was a decrease in FPSII in traps but not in
laminae (Figs 1D, and 2A, B). The rapid changes of FPSII
are not related to the changes in trap geometry caused by
closing, because inhibition of FPSII also occurred in traps
that did not snap after single trigger hair stimulation. This
type of experiment revealed that the inhibition of FPSII is confined mainly to the abaxial side of the trap (Fig. 3). The recovery of FPSII was not entirely completed within 10 min
although the values are only slightly lower (about 0.04) than
before stimulation (Figs 1D, 2A and 3). The inhibition of
FPSII was not as great as inhibition of AN, suggesting that
RD may be transiently enhanced during irritation, because AN
is a function of RD as well as of gross photosynthesis (AG).
We repeated the experiments in the dark. Stimulation of
trigger hairs resulted in transient efflux of carbon dioxide
from traps but not from laminae (Fig. 4). The recovery of RD

Traps
------ Laminae

140
120
100
80
60
40
20
0
100

Traps
Laminae
0

100 200 300 400 500 100

Time (s)

100 200 300 400 500

400
350
300
250
200
150
100
50
0
08
07
06
05
04
03
02
01
0
600

PSII

gs (mmol m2 s1)

8
7
6
5
4
3
2
1
0

R E S ULT S

Ci (L L1)

AN (mol m2 s1)

Chlorophyll fluorescence imaging, measured by the

Fluorcam FC-1000 LC attached to the PLC6 cuvette, was
used to assess the spatiotemporal variations of FPSII by the saturation pulse method. The laminae and traps inside the cuvette
were adapted for 5 10 min to 100 mmol m22 s21 PAR before
the stimulation. Saturation pulses were given every 35 s
(4000 mmol m22 s21 PAR, 800 ms duration) for determination
of FPSII. The three pulses were applied before the trap was
stimulated. The fourth pulse followed 1 2 s after trigger
hairs were irritated and then every 35 s for 10 min (snap
phase) or 15 min (prey struggle phase). Effective quantum
yield was calculated as (Fm0 Ft)/Fm0 (Maxwell and

Johnson, 2000). The changes in FPSII were most pronounced

at low light intensity (100 mmol m22 s21 PAR), when FPSII
values are higher (more light absorbed by PSII is used for
photochemistry) than at high light intensity; therefore, FPSII
was not measured simultaneously with gas exchange at
saturating irradiance.

Time (s)

F I G . 1. Typical responses in Venus flytrap (Dionaea muscipula) of (A) net photosynthetic rate (AN), (B) intercellular CO2 concentration (ci), (C) stomatal conductance (gs) and (D) effective quantum yield of PSII (FPSII) upon stimulation of trigger hairs in traps. Laminae and traps as indicated. The arrows denote the
stimulation of trigger hairs and trap closing.

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0 mmol m22 s21 PAR. Light was provided by blue and red
light-emitting diodes (LEDs) using the Fluorcam FC-1000
LC (Photon Systems Instruments, Brno, Czech Republic)
attached to the PLC6 cuvette. During illumination, the
camera allowed movement of the wire and trap to be monitored inside the cuvette during irritation. The traps or
laminae were kept in the cuvette for 5 10 min (until
steady-state CO2 concentrations were reached) before the
trap (inside or outside the cuvette) was stimulated. After stopping stimulation of the trap, gas exchange measurements continued for an additional 10 min. All parameters were recorded
every 2 s. The area of the trap or lamina did not usually cover
the entire cuvette area, therefore their areas were determined
after the measurement from the recorded images, using the
calibrated Flourcam FC-1000 LC, and gas exchange rates
per unit surface area of trap and lamina were calculated.
Live prey could not be used in our experiments due to their
respiration which would have affected gas exchange
measurements.

Page 3 of 8

Pavlovic et al. Photosynthesis during trap closure in Venus flytrap

Page 4 of 8
A

33 s

2s

37 s

72 s

107 s

142 s

04
177 s

212 s

317 s

422 s

527 s

2s

37 s

72 s

107 s

06

08

PSII

142 s

04
177 s

212 s

317 s

422 s

06

08

PSII

527 s

F I G . 2. Spatiotemporal changes of effective quantum yield of PSII (FPSII) in Venus flytrap assessed by chlorophyll fluorescence imaging of the trap (A) and of
the lamina (B) during trap closure. Green spots in the top left corner denote the stimulation of trigger hairs. Note that the trap snapped.

33 s

2s

37 s

72 s

107 s

142 s

04
177 s

212 s

317 s

422 s

527 s

06

08

PSII

F I G . 3. Spatiotemporal changes of effective quantum yield of PSII (FPSII) in Venus flytrap assessed by chlorophyll fluorescence imaging of the trap after a
single touch of a trigger hair. A green spot in the top left corner denotes the stimulation of a trigger hair. Note that despite the trap not snapping, FPSII decreased.

was completed within 10 min. Similar to the experiments in

the light, ci transiently increased in the traps and stomatal conductance was not affected (data not shown).
After rapid closure secures the prey, mechanical stimulation
of the trigger hairs due to its struggling continues until the prey
is exhausted or dead. Therefore, we continuously measured gas
exchange and chlorophyll fluorescence with mechanical irritation of traps for 5 min: the trigger hairs on the inner
surface were touched by the wire, thus simulating the struggling of prey. Repeated mechanical irritation of trigger hairs
resulted in a rapid decline of AN in traps, to below the CO2
compensation point, so that negative values occurred compared with the snap phase experiment. However, with prolonged stimulation, the suppression of AN slightly decreased.

Again, no inhibition of AN was found in the laminae

(Fig. 5A). Similar to snap phase experiments, gs was not
affected and ci transiently increased (data not shown). FPSII
dropped and the recovery started in parallel with AN after
stimulation (Fig. 5B). The decrease of FPSII in both experiments was due to the decrease of maximum fluorescence
(Fm0 ) as well as to an increase of steady-state fluorescence
(Ft) in the light-adapted state. Chlorophyll fluorescence
showed a substantial decrease of FPSII in traps but not in
laminae. The strongest inhibition of FPSII in traps occurred
in the third zone covered with digestive glands. Reduction of
FPSII in the midrib as well as in the first zone with marginal
teeth and in the second zone with nectar glands was negligible
(Fig. 6A, B). The experiment was repeated in the dark,

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33 s

Pavlovic et al.Photosynthesis during trap closure in Venus flytrap

confirming that both inhibition of the light reactions of photosynthesis and increased RD contribute to the rapid efflux of
CO2 from traps during prey retention. The most rapid efflux
of CO2 was during the first seconds of stimulation.
Prolonged mechanical stimulation decreased the efflux of
CO2. The recovery of RD was also completed within 10
min., similarly to snap phase trap experiments (Fig. 5C).

4
Traps
------ Laminae
RD (mol m2 s1)

Page 5 of 8

DISCUSSION
1

0
100

100

200

300

400

500

600

Time (s)

s1)
AN (mol

m2

8
7
6
5
4
3
2
1
0
1
2
08

Traps
------ Laminae

07
fPSII

06
Traps
Laminae

05
04
03
02
01
00

Traps
------ Laminae

RD (mol

m2

s1)

2
1
0
100 0 100

300

500
700
Time (s)

900

1100

F I G . 5. Typical response of (A) net photosynthetic rate (AN), (B) effective

quantum yield of PSII (FPSII) and (C) rate of respiration (RD) in Venus
flytrap upon repeated stimulation of trigger hairs in closed traps. Laminae
and traps as indicated. The arrows denote the beginning of irritation. The
end of irritation is denoted by a blunt-ended arrow.

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F I G . 4. Rate of respiration (RD) in Venus flytrap upon stimulation of trigger

hairs. Laminae and traps as indicated. The arrow denotes the stimulation of
trigger hairs and trap closing.

The results show unequivocally that stimulation of trigger

hairs in D. muscipula rapidly decreased AN in traps but not
in laminae (Fig. 1A), and chlorophyll fluorescence imaging
also showed a decrease of FPSII in traps, but not in the
laminae (Fig. 2A, B). Therefore, light, as well as dark, reactions of photosynthesis were inhibited during trap closure.
We are convinced that reduction of photosynthesis in the
Venus flytrap is due to irritation of trigger hairs which generate
electrical signals and is independent of trap closure: single
hair irritation and the prey struggle phase of the experiment
also resulted in reduction of photosynthesis (Figs 3, 5A, B and
6A). Action potentials in Dionaea have been extensively
studied (Burdon-Sanderson, 1873; Hodick and Sievers, 1988;
Hodick and Sievers, 1989; Sibaoka, 1991; Krol et al., 2006;
Volkov et al., 2007). Action potentials propagate from
mechano-sensitive trigger hairs of the lobe to the midrib in
the traps. Volkov et al. (2007, 2008a) concluded that action
potential signalling in Dionaea is limited to the traps and is
not propagated to the laminae. Only graded potentials with
very low amplitude were detected 2 min after the trap
closing in laminae, and these electrical signals have no
effect on AN, RD or FPSII in laminae (Figs 1, 2 and 4 6). A
graded potential is a wave of electrical excitation that
appears as a result of short-lived depolarization or hyperpolarization of an area of the plasma membrane in conductive
bundles of plants. Graded potentials become weaker as they
travel along conductive bundles in plants, whereas action
potentials remain the same strength as they travel. Inhibitory
effects of electrical signals on photosynthesis have been documented in different plant species (Fromm and Eschrich, 1993;
Koziolek et al., 2003; Lautner et al., 2005; Bulychev and
Kamzolkina, 2006; Hlavackova et al., 2006; Kaiser and
Grams, 2006). However, the mechanisms causing photosynthetic limitation by electrical signals are poorly understood.
Subcellular alterations in ion fluxes may be involved
(Lautner et al., 2005). In most studies, the response was
induced by heat stimulation, and photosynthesis was measured
in neighbouring leaves. In the case of the sensitive plant
Mimosa pudica, reduction of net CO2 exchange and FPSII in
a neighbouring leaf is much stronger than observed in other
plant species, and stomatal conductance rapidly increases
during the first 2 min after heat stimulation, and subsequently
declines to approximately half of the initial value before heat
stimulation (Koziolek et al., 2003; Kaiser and Grams, 2006).
A rapid decline in stomatal conductance and photosynthesis
in neighbouring leaves after heat stimulation also occurs in
tobacco (Hlavackova et al., 2006). In our experiment with
Dionaea, no reactions of stomata after mechanical stimulation
were observed; therefore, we can exclude stomatal limitation
of photosynthesis (Fig. 1C). Moreover, rapid efflux of CO2

Pavlovic et al. Photosynthesis during trap closure in Venus flytrap

Page 6 of 8
A

33 s

2s

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422 s

04
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632 s

737 s

842 s

947 s

2s

107 s

212 s

317 s

06

08

PSII

422 s

04
527 s

632 s

737 s

842 s

947 s

06

08

PSII

F I G . 6. Spatiotemporal changes of effective quantum yield of PSII (FPSII) in Venus flytrap assessed by chlorophyll fluorescence imaging of the trap (A) and of
the lamina (B), respectively, during repeated stimulation of trigger hairs in closed traps, thus simulating the struggling prey. Green spots in the top left corner
denote the beginning of trigger hair stimulation; the red spots denote the end of stimulation.

in the dark indicates a transient increase of RD (Fig. 4).

Therefore, it seems unlikely that changes in light and dark
reactions of photosynthesis alone can explain the rapid
decline of AN. A transient increase in RD after an electrical
and damaging stimulus was found in the liverwort
Conocephalum conicum (Dzubinska et al., 1989). In addition,
significant amounts of ATP are hydrolysed in the midrib of
D. muscipula during trap closure (Jaffe, 1973). Williams and
Bennett (1982) confirmed that during the closure about 29 %
of the cellular ATP is lost; this is used for rapid transport of
hydrogen and water, resulting in changes in turgor pressure
and subsequent closure of the trap. However, data presented
here indicate that enhanced RD is not only associated with
the energy needed for trap closure, because increased RD
also occurred during repeated mechanical irritation of trigger
hairs in closed traps (Fig. 5C).
The cost/benefit model of carnivory proposed by Givnish
et al. (1984) predicts that carnivorous plants grow in nutrientpoor, but sunny and wet habitats, because only in this environment would the cost of producing traps be lower than the
benefits gained from prey. Benefit from carnivory in term of
increased AN, as a result of increased mineral absorption
from prey, was confirmed only recently (Farnsworth and
Ellison, 2008; Pavlovic et al., 2009). In addition, costs represent energy devoted to carnivory in term of lures and digestive enzymes as well as lower AN in traps, relative to
non-carnivorous organs (reviewed by Ellison and Gotelli,
2001; Ellison, 2006; Ellison and Gotelli, 2009). Several
authors also include in the costs increased RD of carnivorous

organs (Knight, 1992; Adamec, 2006). Laakkonen et al.

(2006) modified the model of Givnish et al. (1984) by replacing photosynthetic with respiratory costs in Utricularia,
because RD in Utricularia bladders was 75 200 % greater
than that in the leaves (Adamec, 2006). Adamec (2006)
suggested that bladders were probably in a post-firing state
and pumping water. As demonstrated by Sydenham and
Findlay (1975), ion and water pumping during the resetting
of Utricularia bladders is a process requiring considerable
energy, derived from respiration. However, there are no
direct measurements of CO2 exchange in relation to resetting
of bladders or trapping prey. The costs of carnivory have
been assessed much less frequently than the benefits,
because measuring energy lost is more difficult than measuring
the benefits (Ellison and Gotelli, 2009). Until now, studies
assessing the costs of carnivory have usually been confined
to measurements of AN and RD in carnivorous traps vs. noncarnivorous leaves (Knight, 1992; Ellison and Gotelli, 2002;
Adamec, 2006; Pavlovic et al., 2007; Karagatzides and
Ellison, 2009; Hajek and Adamec, 2010), to the construction
costs and payback times for carnivorous organs (Osunkoya
et al., 2007; Osunkoya et al., 2008; Karagatzides and
Ellison, 2009) or to the carbon costs of sticky mucilage
secretion by glands (Thoren et al., 2003). Taking into
account the classical interpretation of the cost/benefit model,
Ellison and Gotelli (2009) suggest that the Dionaea trap is
an inexpensive structure. Our results demonstrate that rapid
movement of traps is costly. Moreover, struggling prey
closed inside the trap mechanically stimulate trigger hairs,

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33 s

Pavlovic et al.Photosynthesis during trap closure in Venus flytrap

Transport of
assimilates?
Lamina

Trap, construction
costs, decreased AN

Insect trapping and

retention, decreased
AN, increased RD
Sunny, wet habitat
Shade, dry habitat

Benefit from prey,

stimulation of AN
in lamina

generating electrical signals which further inhibit AN and

FPSII, and stimulate RD (Fig. 5). That entrapped prey stimulate
the trigger hairs and result in generation of action potentials
was shown by Affolter and Olivo (1975). Lichtner and
Williams (1977) elicited action potentials in traps for .5 h
using nylon bristles. This indicates that inhibition and stimulation of AN and RD, respectively, may continue until the
prey enclosed in the trap stops moving and may represent substantial carbon costs, especially at night or at low light intensities, when AN is limited. Thus the prevailing cost/benefit
model of carnivory requires modification to include photosynthetic responses directly associated with prey capture and
retention (Fig. 7).
Darwin (1875) observed that small gaps between marginal
teeth after rapid closure of the lobes of the leaf to form the
trap allow small prey to escape from traps. This could be an
adaptive trait, saving energy, because small prey do not
provide sufficient amounts of nutrients to benefit the plant in
terms of increased AN and to outweigh the costs associated
with retention of prey in a closed trap (decreased AN
increased RD). Gibson and Waller (2009) hypothesize that
snap-traps evolved from flypaper (sticky) traps to capture
and digest larger prey efficiently, which brings greater
benefit. The classical cost/benefit model considers a constant
rate of CO2 exchange with no direct photosynthetic costs
associated with prey capture and retention (the plant is considered a passive creature with small AN, and in some
species with higher RD in traps). We provide a new insight
into the cost/benefit model of carnivory, showing variable
flux of CO2 in relation to prey capture and retention (the
plant as an active creature) that may also apply to other carnivorous species. Generation of action potentials after mechanical stimulation was also found in the genus Drosera (Williams
and Pickard, 1972a, b, 1974) and their effect on CO2 metabolism is highly likely. Our preliminary observations using
chlorophyll fluorescence imaging confirmed reduction of
FPSII in response to prey addition in Drosera capensis. Also,

dynamic changes in CO2 metabolism during resetting and

movement of Utricularia bladder are expected.
In conclusion, we showed for the first time that irritation of
trigger hairs, which is usually associated with prey capture and
retention in the carnivorous plant D. muscipula, resulted in
rapid downregulation of photosynthesis and stimulation of respiration probably via electrical signals. The limitation of
photosynthesis was not associated with a decrease in stomatal
conductance, but was due to the decrease of utilization of
absorbed light energy by chlorophylls for photochemistry or
by a decrease in activity of enzymes of the Calvin cycle,
which affect FPSII by a feedback mechanism. We modified
the classical interpretation of the cost/benefit model of carnivory by including the CO2 costs directly associated with prey
capture and retention. Further studies are required to assess
the direct costs associated with prey capture and retention
and their effect on the daily carbon gains in carnivorous plants.
ACK NOW LED GE MENTS
This work was supported by grant VEGA 1/0040/09 from the
Scientific Grant Agency of the Ministry of Education of the
Slovak Republic.
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F I G . 7. Schematic modified cost/benefit model of carnivory, associated with

insect trapping and retention. Traps bearing some construction costs
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