Harmless nectar source or deadly trap: Nepenthes pitchers are activated by rain, condensation and nectar.
ABSTRACT The leaves of Nepenthes pitcher plants are specialized pitfall traps which capture and digest arthropod prey. In many species, insects become trapped by 'aquaplaning' on the wet pitcher rim (peristome). Here we investigate the ecological implications of this capture mechanism in Nepenthes rafflesiana var. typica. We combine meteorological data and continuous field measurements of peristome wetness using electrical conductance with experimental assessments of the pitchers' capture efficiency. Our results demonstrate that pitchers can be highly effective traps with capture rates as high as 80% but completely ineffective at other times. These dramatic changes are due to the wetting condition of the peristome. Variation of peristome wetness and capture efficiency was perfectly synchronous, and caused by rain, condensation and nectar secreted from peristome nectaries. The presence of nectar on the peristome increased surface wetness mainly indirectly by its hygroscopic properties. Experiments confirmed that pitchers with removed peristome nectaries remained generally drier and captured prey less efficiently than untreated controls. This role of nectar in prey capture represents a novel function of plant nectar. We propose that the intermittent and unpredictable activation of Nepenthes pitcher traps facilitates ant recruitment and constitutes a strategy to maximize prey capture.
- SourceAvailable from: amjbot.org[show abstract] [hide abstract]
ABSTRACT: The pitchers of the tropical carnivorous plant Nepenthes alata are highly specialized organs for the attraction and capture of insects and absorption of nutrients from them. This study examined the structure and development of these pitchers, with particular focus on the nectaries and digestive glands. Immature pitchers developed at the tips of tendrils and were tightly sealed by a lid structure that opened during the end of pitcher elongation. Opened pitchers exposed a ridged peristome containing large nectaries. Like other members of the genus, a thick coating of epicuticular waxy scales covered the upper one-third of the pitcher. Scattered within this zone were cells resembling a stomatal complex with a protruding ridge. Cross sections showed that this ridge was formed by asymmetric divisions of the epidermal cells and lacked an underlying pore. The basal region of the trap had large multicellular glands that developed from single epidermal cells. These glands were closely associated with underlying vascular traces and provided a mechanism for supplying fluid to closed immature pitchers.American Journal of Botany 11/1999; 86(10):1382-90. · 2.59 Impact Factor
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ABSTRACT: Field studies have indicated that bolas spiders attract male moth prey, apparently by mimicking the odor of female moth sex pheromones. Three moth sex pheromone compounds, (Z)-9-tetradecenyl acetate, (Z)-9-tetradecenal, and (Z)-11-hexadecenal, were identified in volatile substances emitted by hunting adult female Mastophora cornigera spiders. These compounds are components of pheromone blends that attract some of this spider's moth prey species.Science 06/1987; 236(4804):964-7. · 31.03 Impact Factor
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ABSTRACT: The slippery zone situated below the peristome inside pitchers of most carnivorous plants from the genus Nepenthes is covered with a thick layer of epicuticular wax. This slippery zone is reported to play a crucial role in animal trapping and prey retention. In N. alata, the wax coverage consists of two clearly distinguished layers. These layers differ in their structure, chemical composition and mechanical properties, and they reduce the insect attachment in different ways. The lower layer resembles foam, composed of interconnected membraneous platelets protruding from the surface at acute angles. The upper layer consists of densely placed separate irregular platelets, located perpendicular to the subjacent layer. Crystals of the upper layer bear small stalks, directed downwards and providing connections to the lower layer. These morphological distinctions correlate with differences in the chemical composition of waxes. The compound classes of alkanes, aldehydes, primary alcohols, free fatty acids, esters and triterpenoids occurred in extracts from both wax layers, but in different proportions. Chain length distributions in aliphatics were different in extracts from the lower and the upper wax layers. Waxes of the upper and lower layers exhibited different mechanical properties: wax of the lower layer is harder and stiffer than that of the upper layer. Moreover, crystals of the upper layer are brittle and may be easily exfoliated or broken to tiny pieces. Laboratory experiments using tethered insects showed that both wax layers reduce the attachment force of insects. It is assumed that a decrease in insect attachment on the two distinct wax layers is provided by the two different mechanisms: (1) crystals of the upper wax layer contaminate insects' adhesive pads; (2) the lower wax layer leads to a reduction of the real contact area of insects' feet with the plant surface.Journal of Experimental Biology 01/2006; 208(Pt 24):4651-62. · 3.24 Impact Factor
Harmless nectar source or deadly trap:
Nepenthes pitchers are activated by rain,
condensation and nectar
Ulrike Bauer, Holger F. Bohn and Walter Federle*
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
The leaves of Nepenthes pitcher plants are specialized pitfall traps which capture and digest arthropod prey.
In many species, insects become trapped by ‘aquaplaning’ on the wet pitcher rim (peristome). Here we
investigate the ecological implications of this capture mechanism in Nepenthes rafflesiana var. typica. We
combine meteorological data and continuous field measurements of peristome wetness using electrical
conductance with experimental assessments of the pitchers’ capture efficiency. Our results demonstrate
that pitchers can be highly effective traps with capture rates as high as 80% but completely ineffective at
other times. These dramatic changes are due to the wetting condition of the peristome. Variation of
peristome wetness and capture efficiency was perfectly synchronous, and caused by rain, condensation and
nectar secreted from peristome nectaries. The presence of nectar on the peristome increased surface
wetness mainly indirectly by its hygroscopic properties. Experiments confirmed that pitcherswith removed
peristome nectaries remained generally drier and captured prey less efficiently than untreated controls.
This role of nectar in prey capture represents a novel function of plant nectar. We propose that the
intermittent and unpredictable activation of Nepenthes pitcher traps facilitates ant recruitment and
constitutes a strategy to maximize prey capture.
Keywords: carnivorous plants; extrafloral nectar; leaf wetness; aquaplaning
The interaction between predators and their prey has led
to the evolution of adaptive strategies on both sides
(Driver & Humphries 1988; Krebs & Davies 1997;
Barbosa & Castellanos 2005). Most predators belong to
the animal kingdom, but there are also several plant genera
which have adopted carnivory as a means of acquiring
nitrogen in nutrient-poor habitats. Carnivorous plants
have evolved sophisticated adaptations to capture arthro-
pod prey (Lloyd 1942; Juniper et al. 1989; Ellison &
Gotelli 2001). In contrast to animal predators that spend
only a fraction of their time hunting, traps of carnivorous
plants are usually active all the time. The palaeotropic
genus Nepenthes (Nepenthaceae) comprises more than 80
species of pitcher plants (Jebb & Cheek 1997). The leaves
of these plants are mug-shaped organs specialized for
attracting, capturing, retaining and digesting the prey.
Arthropods attracted by extrafloral nectar and optical/
olfactory cues (Moran 1996; Moran et al. 1999; Merbach
et al. 2001) lose their foothold and fall into the digestive
fluid which fills the lower part of the pitcher (Clarke &
Several capture mechanisms have been proposed for
Nepenthes pitchers. First, trapping is thought to be based
on a slippery wax bloom on the inner pitcher wall of many
Nepenthes species (Knoll 1914; Lloyd 1942; Juniper &
Burras 1962; Juniper et al. 1989; Moran et al. 1999;
Gaume et al. 2002). It is made up of microscopic,
epicuticular wax crystal platelets which give rise to anti-
adhesive surface roughness and easily break off, thus
contaminating attachment structures and causing arthro-
pods to slip (Knoll 1914; Juniper & Burras 1962; Gorb
et al. 2005). Second, it has been suggested that anaesthesia
by narcotic alkaloids causes prey capture in Nepenthes
madagascariensis (Ratsirarson & Silander 1996). Only
recently, we discovered that many Nepenthes species
capture prey with the upper pitcher margin (the
peristome, figure 1a,b; Bohn & Federle 2004). Its surface
is characterized by a regular microstructure with radial
ridges of smooth overlapping epidermal cells, which form
a series of steps towards the pitcher inside (Owen &
Lennon 1999). The peristome ridges mostly extend into
tooth-like structures at the inner edge, in between which
large extrafloral nectaries are situated. The micro-
structure, combined with hydrophilicity, renders the
peristome completely wettable, in contrast to most other
plant surfaces. Water droplets spread rapidly and form
homogeneous thin films, which make the peristome
extremely slippery for insects. When the peristome is
wet, the fluid films prevent the insects’tarsal adhesive pads
from making close contact with the surface, similar to the
aquaplaning of a car tyre on a wet road. In addition, the
anisotropic microstructure of the peristome surface allows
interlocking of claws only while the insect is running
towards the pitcher inside, but not on the wayout (Bohn &
This wetness-based capture mechanism of Nepenthes
pitcher plants has interesting ecological implications. As
dry peristomes are not slippery for insects (Bohn &
Federle 2004), pitchers only work as effective insect traps
Proc. R. Soc. B (2008) 275, 259–265
Published online 29 November 2007
Electronic supplementary material is available at http://dx.doi.org/10.
1098/rspb.2007.1402 or via http://journals.royalsociety.org.
*Author for correspondence (email@example.com).
Received 11 October 2007
Accepted 6 November 2007
This journal is q 2007 The Royal Society
when their peristomes are wet. However, it is still unclear
when and how this is achieved under natural conditions.
Water films on the peristome may originate from rain,
condensation and nectar secretion, of which only the last
mechanism provides the possibility of an active regulation
by the plant. The interaction of all three factors could lead
to a complex pattern of trap activation. Here we study the
temporal variation of peristome wetting and capture
efficiency in the field. We investigate (i) when and by
which mechanism peristomes are wetted under natural
conditions and (ii) whether pitcher trapping efficiency
changes with daytime and weather conditions as predicted
from the condition of the peristome.
2. MATERIAL AND METHODS
Experiments were performed on Nepenthes rafflesiana var.
typica at a site with heavily degraded kerangas forest on white
sandy soil in Brunei, northern Borneo (48340N, 1148250E).
The vegetation is open, and temperatures ranged from 248C
in late night to 388C in early afternoon. N. rafflesiana
var. typica is abundant and occurs sympatrically with
(a) Measurement of peristome wetness using
We developed a method to continuously monitor the wetness
of pitcher peristomes in the field. It was determined from the
resistance between two electrodes attached to the inner and
outer margins of the peristome. The inner contact was held in
position by a tiny magnet. Its lead was passed to the outside
through a small hole in the pitcher wall. The outer contact
was a small spring with a V-shaped tip. It was mounted on a
plastic holder which was attached to the pitcher using
adhesive tape (figure 1c,d).
An electrical circuit containing a potential divider with a
fixed resistor of 1 MU was used to record the electrical
resistance of the peristome as a voltage (figure 1d and
electronic supplementary material, figure S3). The circuit
used AC with UZ12Vppand a frequency of 1 kHz. Data were
recorded from several pitchers simultaneously with a
sampling frequency of 1 minK1using a mLog VL 100S
eight-channel data logger (a.b.i. data, Brussels). Voltage
values were converted to conductance according to the
where Rpis the peristome resistance; Rfis the fixed resistor;
and Umeasured is the measured voltage. The electrical
conductance reflects the degree of surface wetting. We
of 24 hours with that of visual assessments of peristome
wetness on 30 pitchers (16 checks in intervals of 90 min). We
classified the observed states of peristome wetness in four
categories ranging from completely dry to wet (continuous
fluid film on the surface). The results of conductance
measurements and personal observations were strongly
correlated (Spearman’s rank test: nZ16, d.f.Z14, rZ0.80,
p!0.01). Owing to variable electrolyte content of the fluid on
the peristome surface and the non-standardized distance and
contact area of the electrodes, our method does not allow
conclusions about the absolute amount of fluid present (cf.
Klemm et al. 2002). However, since the position of electrodes
remained constant during the experiments, temporal vari-
ations of peristome wetness could be reliably recorded.
In addition to the measurements of peristome wetness, we
continuously recorded air temperature and relative humidity
using Tinytag Plus data loggers (Gemini Data Loggers,
Chichester), and monitored precipitation with a tipping
bucket rain gauge (Rain Collector II, Davis Instruments
Figure 1. (a) Upper pitcher of Nepenthes rafflesiana var. typica (p, peristome; n, position of peristome nectaries). (b) SEM image
showing the regular microstructure of the peristome. Scale bar, 500 mm. (c) Peristome of upper pitcher of N. rafflesiana var.
typica with magnetic electrode (inside) and spring electrode (outside). (d) Schematic of experimental setup used to measure the
wetness of the peristome. The electrical resistance between both electrodes provides a measure of the degree of peristome
260 U. Bauer et al. Harmless nectar source or deadly trap
Proc. R. Soc. B (2008)
Corp., Hayward) connected to one channel of the mLog VL
100S data logger.
(b) Measurement of capture efficiency
To bring large numbers of ants into contact with N. rafflesiana
pitchers, we collected partial colonies (50–300 workers) of a
Camponotus species belonging to the C. (Colobopsis) saundersi
group (body length approx. 10 mm) on the day before the
experiments. We kept them (fed with honey–water) in plastic
containers side-coated with slippery Fluon (Whitford, Diez)
to prevent ants from escaping. To start the experiment, live
N. rafflesiana pitchers were placed upright on a support inside
the plastic container so that the ants had access. The ants ran
onto the pitchers to explore the new object, that is, they were
not foraging for food. We investigated whether experimental
wetting of the peristome in N. rafflesiana var. typica pitchers
increased the capture efficiency, as we demonstrated pre-
viously for Nepenthes bicalcarata (Bohn & Federle 2004). We
tested the effects of wetting (using an atomizer), drying (with
dust-free tissue) and re-wetting (see figure S1 and video in the
electronic supplementary material).
To investigate the correlation of peristome surface
conductance and trapping efficiency, we performed consecu-
tive running experiments and simultaneous voltage measure-
ments on the same pitchers in the field. The digestive fluid
was removed for the duration of the experiment to reduce the
consumption of test animals. The ants were recorded while
running on the pitcher using a Sony DCR-PC120E video
camera. Videotapes were analysed by counting the number of
capture events in relation to the number of peristome visits. A
visit was defined as an ant stepping onto the peristome with
more than three legs, no matter if the peristome was entered
from the inside or the outside. Re-entering of the peristome
was counted as a new visit. This definition ensured that all
ants were counted that could potentially be trapped. Other,
more rigorous definitions (e.g. all legs in contact with the
peristome) would have led to even more clear-cut effects.
(c) Experiments on pitchers with removed
To evaluate the contribution of nectar secretion to peristome
wetting, we abscised the peristome nectaries of two pitchers.
This was achieved by cutting an approximately 3 mm wide
strip off the inner margin of the peristome using a fine scalpel.
Even though this treatment lowered the capture rate, pitchers
devoid of peristome nectaries were still highly effective insect
traps when wet (see figure S2 in the electronic supplementary
material). We monitored peristome conductance of these
pitchers simultaneously with that of two unmanipulated
control pitchers on the same plants. This experiment was
repeated on another set of 2!2 pitchers one month later. To
differentiate between the direct and indirect effects of nectar
on peristome wetness, we calculated for each pitcher ‘relative
conductances’ ranging from 0 to 100% and determined the
time when the peristomes reached 50% re-wetting in the
afternoon (only days without precipitation analysed). If
pitchers directly wet their peristomes with fluid nectar,
pitchers with abscised nectaries should reach 50% re-wetting
later than intact pitchers. However, if peristome nectar films
mainly originate by rehydration of dried nectar, pitchers with
and without nectaries should reach 50% re-wetting at the
same time which would largely depend on air humidity.
To investigate the relevance of nectar for prey capture, we
performed a series of simultaneous running experiments on
three differently treated pitchers growing on the same plant.
On one pitcher, we abscised the nectaries and rinsed the
peristome with distilled water to remove all nectar. The
peristome of the second pitcher was only rinsed, and the third
pitcher remained untreated.
(a) Temporal variation of capture efficiency
The capture efficiency of N. rafflesiana var. typica pitchers
showeda pronounced diurnal variation (figure 2). Pitchers
did not capture any ant during most of the day but they
were highly efficient traps in the evening, night and early
morning (capture efficiency ranging from 0% to more than
80%). The most significant changes in capture rates took
place from 07.00 to 08.00 and from 17.30 to 18.00
(conventional and Craddock–Flood’s chi-squared tests,
p!0.001, for sample sizes see figure 2).
(b) Capture efficiency and peristome wetness
Experimental wetting of the peristome of N. rafflesiana var.
typica pitchers increased the capture efficiency from 0% to
more than 60%, similar to our earlier findings for
N. bicalcarata (Bohn & Federle 2004, see figure S1 in
the electronic supplementary material). Under natural
conditions, daily fluctuations of peristome wetness also
give rise to dramatic changes in capture efficiency, as
revealed by our combined measurements of peristome
surface conductance and capture rate.
Changes in capture efficiency and peristome wetness
were almost perfectly synchronized (figure 2), the corre-
lation between both being positive and highly significant
was not at all slippery for ants. Under wet conditions,
however, most ants slipped and fell into the pitcher as soon
as they stepped onto the peristome.
(c) Effects of rain and condensation
Peristome wetness showed regular diurnal oscillations
with higher conductance during the night (figure 3).
Superimposed on this pattern were peaks caused by
precipitation which generally led to a strong and rapid
increase in surface conductance. Parallel measurements
from the same pitcher and from adjacent, simultaneously
monitored pitchers showed very similar curve pro-
gressions even though their absolute conductance differed
depending on the conditions of the electrode contact.
At times without precipitation, the conductance curve
largely followed the relative air humidity curve. Dew
formation at night was observed regularly. During the
hydrophobic leaf surfaces were densely covered with
dewdrops. The capacity of dew to wet the peristome
sufficiently for prey capture was proven in running
experimentswithants onpitcherswithout nectaries during
a rainless night (figure 5c). In this experiment, all other
possible sources of wetting but dew had been excluded.
(d) Effect of peristome nectar
In the evening hours, we regularly observed large amounts
of liquid nectar on the peristomes of N. rafflesiana var.
typica, suggesting that nectar secretion plays an important
role in the wetting of the peristome. We tested the
Harmless nectar source or deadly trap
U. Bauer et al.
Proc. R. Soc. B (2008)
contribution of nectar by evaluating the effect of nectary
abscission on peristome wetness and prey capture. Visual
assessments and conductance measurements confirmed
that the peristomes without nectaries were distinctly drier
than the control group at most times of the day. Moreover,
the conductance measurements revealed an interesting
phenomenon (figure 4a). In the first days after nectary
abscission, conductance curves of manipulated and
unmanipulated peristomes progressed similarly on a
comparable level (Mann–Whitney U-test of 24th h
means, nZ8, UZ21.0, p[0.05). However, after the
first heavy downpour had rinsed off the nectar, the
conductance curves of manipulated pitchers still showed
the same temporal variation but were shifted to a markedly
lower levelwhile those of unmanipulated pitchers remained
was highly significant (Mann–Whitney U-test of 24 h
means, nZ42, UZ377.0, p!0.001). This indicates that
considerably enhances peristome wetting. The largely
unchanged time course of peristome conductance in
pitchers without nectaries shows that the observed patterns
are not caused by plant-induced variations of nectar
Rain increased the conductance of all peristomes to a
comparable level (figure 4b). Thus, the absence of nectar
had no effect on the wetting by rain, but it decreased water
condensation from the air. Surprisingly, our data provide
no evidence of direct wetting of the peristome surface by
secretion of liquid nectar. In both experiments, the
daytime of 50% re-wetting did not differ significantly
between pitchers with and without peristome nectaries
(Kruskal–Wallis tests: n1Z15, H1Z6.47, p1[0.05;
n2Z9, H2Z2.37, p2[0.05; figure 4c). This suggests
that nectar is mainly secreted at times of high humidity
when the peristome is already fullywetted,that is, between
the evening and early morning. We conclude that even
though nectar plays an important role for peristome
wetting, its contribution is mainly indirect as an enhancer
of water condensation.
The running experiments with ants on pitchers with
different manipulations clearly showed the importance of
nectar for prey capture (figure 5). Removal of the nectaries
had no visible effect on the ants’ behaviour and many
workers were running on the peristome. While both the
unmanipulated and the intact but rinsed pitcher exhibited
the usual increase in slipperiness and trapping efficiency
(pitchers not significantly different at any time; Fisher’s
exact tests for ‘fallen’ versus ‘not fallen’: pO0.05), the
pitcher without peristome nectaries remained completely
ineffective throughout the afternoon (highly significant
differences to pitchers with nectaries at 18.25–18.55 and
19.15–20.00; Bonferroni-corrected Fisher’s exact tests:
p!0.001). Only in the middle of the night did the pitcher
without nectaries also become slippery so that the capture
efficiency of all pitchers was again similar (Fisher’s exact
test: pO0.05). As wetted pitchers with abscised nectaries
are still effective traps (see figure 5c and electronic
supplementary material, figure S2), this effect cannot be
explained by the mechanical effects of the manipulation
n = 43 19
time of day
proportion of ants (%)
Figure 2. Temporal variation of peristome surface conductance and capture rate as obtained in a time series of running
experiments with Camponotus (Colobopsis) sp. ants on a N. rafflesiana var. typica pitcher. Note that the time scale is not evenly
rainfall (mm h–1)
16 May17 May18 May
Figure 3. Diurnal variation of peristome surface conductance
of twoN. rafflesiana var. typica pitchers (top, green and orange
curves), precipitation (top, blue bars) and meteorological
data (bottom, red and blue curves) at the study site in Brunei.
Nights are marked by grey background. High conductance
indicates a wet peristome.
262U. Bauer et al.Harmless nectar source or deadly trap
Proc. R. Soc. B (2008)
but it demonstrates that the peristome nectaries facilitate
prey capture via enhanced water condensation.
(a) Activation of traps by peristome wetting
var. typica pitchers changes dramatically over time.
The close correlation of trapping efficiency and peristome
can be completely attributed to changes in the degree of
peristome wetting. These findings confirm the importance
of the peristome and of ‘insect aquaplaning’ for prey
capturebyNepenthesspecies (Bohn&Federle 2004)under
field conditions. Although the running experiments with
ants did not represent natural capture events, they
accurately indicate the effectiveness of the pitcher traps.
The extreme temporal variation of pitcher capture
efficiency has not been documented previously. It explains
why the trapping function of the peristome has long
remained overlooked (Lloyd 1942; Juniper et al. 1989;
Gaume et al. 2002).
Whyshould acarnivorous plant have evolvedatrapping
mechanism which is often ineffective and thus seemingly
ill designed? It has been suggested that accumulation of
excessive amounts of prey could cause putrefaction and
thus an earlier death of the pitcher (Clarke & Kitching
1995). On the other hand, prey digestion is known to be
accomplished to a large degree by the pitcher infauna
under natural conditions (Bradshaw & Creelman 1984)
and pitchers can capture vast amounts of prey without
being harmed (Merbach et al. 2007). Therefore, it seems
unlikely that there is a selective pressure for prey reduction
in Nepenthes. On the contrary, we propose that the
temporary ineffectiveness of the trap is actually a strategy
for maximizing prey capture. Surprise and unpredict-
ability are essential elements of animal hunting behaviour
(e.g. Driver & Humphries 1988). Animal predators show
behavioural adaptations that make them difficult to detect
and unpredictable, such as irregular hunting, aggressive
mimicry (e.g. Stowe et al. 1987), stalking behaviour and
ambushing. Besides the direct advantage gained by a
surprise attack, the unpredictability of predator behaviour
will make the evolution of specific avoidance behaviours
more difficult, and thus ensure sustained prey capture
success in the long term.
The trapping in N. rafflesiana var. typica pitchers bears
interesting parallels to the strategies of animal predators.
Although the general pattern of diurnal variation of
peristome wetness was largely consistent over time, the
exact state of wetting at a given time varied from dayto day
and between pitchers, due to changes in weather
conditions and spatial variations in microclimate. Many
Nepenthes species (e.g. N. bicalcarata) thrive in less open
and more humid habitats than our study site. In these
habitats, the diurnal variation of humidity is less regular
and less predictable. As a consequence, pitcher-visiting
insect species cannot easily counteradapt and avoid being
trapped simply by restricting foraging to a particular time
of day. Similarly, on an individual scale, insects can hardly
learn to avoid pitcher plants because they mostly die from
their first negative experience.
Nepenthes pitcher plants might also benefit more
directly from the temporary ineffectiveness of the trap. A
major proportion of prey in most Nepenthes species
consists of ants (Jebb 1991; Moran 1996), which can
efficiently exploit patchy food resources by recruiting
nestmates (Ho ¨lldobler & Wilson 1990). Tan (1997)
proposed that low pitcher capture rates in general should
result in a greater number of surviving ‘scout’ ants, which
then recruit more nestmates to the pitchers. Therefore,
low capture efficiency might ultimately result in increased
prey numbers. However, our findings suggest that the
variable capture efficiency results in a temporal separation
of ant (scout) attraction by nectar and the capture of
recruited nestmates.Such a strategy might yield more prey
than a continuously low capture efficiency.
(b) Natural sources of peristome wetting
The conductance measurements revealed that all three
possible mechanisms of peristome wetting—rain, dew and
nectar secretion—operate in N. rafflesiana var. typica. The
impact of rain was particularly obvious in recordings of
daytime rainfalls (figure 4b). Even though the pitcher lid
shields the pitcher sufficiently against flooding, it does not
prevent the peristome from being wetted by rain. A
possible consequence of the pitcher activation by rainfall is
that pitchers capture more prey during rainy seasons,
time of day
3 May 4 May 5 May 6 May 7 May 8 May
Figure 4. (a) Comparison of peristome surface conductance
of N. rafflesiana var. typica pitchers with (green curve) and
without (red curve) peristome nectaries (means plotted).
Nights are marked by grey background. Nectaries were
abscised on 2 May. Both curves diverge markedly after the
first heavy rain (arrow). (b) Later stage of the same
experiment. Rainfall (black arrows) increases the conduc-
tance of both groups of peristomes to about the same level
(light daytime rainfall on 10 May not recognized by the rain
gauge). (c) Daytimes of 50% peristome re-wetting in pitchers
with (green boxes) and without (red boxes) peristome
nectaries. Pitchers 1–4 were monitored from 27 March to 2
May 2006 and pitchers 5–8 from 2 May to 20 May 2006.
Harmless nectar source or deadly trap
U. Bauer et al.
Proc. R. Soc. B (2008)
which may also be periods of faster growth and greater
demand of nutrients.
At times without precipitation, peristome conductance
largely followed the diurnal changes of air humidity. The
open vegetation at our study site and the resulting wide
range of temperatures measured in the diurnal cycle
(figure 2) entailed pronounced oscillations of relative air
humidity and thus enhanced the diurnal variation of
peristome wetness and capture efficiency. Measurements
and observations on pitchers without nectaries clearly
confirmed that high air humidity at night is sufficient to
wet the peristomes.
The comparison of pitchers with and without nectaries
demonstrated the importance of nectar for peristome
wetting. We were able to show that the main contribution
of nectar towards peristome wetting is indirect by
facilitating water condensation, while an influence of
direct wetting could not be shown. Sugar and nectar
are well known for their hygroscopic properties
(Browne 1922), and spot checks of freshly secreted
peristome nectar in N. rafflesiana var. typica indicated
high sugar concentrations of 10–40% (W. Federle 2005,
unpublished results). Owing to its spreading on the
completely wettable peristome surface, the nectar is
exposed to wind and sunshine which facilitate eva-
poration. This is in striking contrast to the extrafloral
nectaries of many other plants which are often cup-shaped
and designed to minimize evaporation in order to keep the
nectar attractive and consumable to insects (Elias 1983).
Evaporation can lead to nectar crystallizing at daytime and
becoming liquid again by water absorption at night
(Deppe et al. 2000). During hot and dry days, we regularly
observed dried nectar on the peristome surface of
in the re-wetting of the peristome, nectar evaporation
(mediated by the structure of the peristome) may be less
adversarial for Nepenthes than it is for other plants. Despite
possible that pitcher plants actively regulate the degree of
wetting by adjusting the amount of nectar secretion.
The role of nectar in prey capture in Nepenthes is
remarkable because it involves a novel, purely mechanical
function of nectar. Usually, nectar is used by plants to
attract and/or reward insects in the context of pollination
and biotic defence (Herrera & Pellmyr 2002; Wa ¨ckers
et al. 2005). The nectar in N. rafflesiana var. typica also
serves the attraction of prey insects. However, its function
to increase the mechanical efficiency of the pitcher trap
represents the acquisition of a new role. Further studies
should establish whether the peristome nectar in
Nepenthes, owing to its exceptional function, differs in its
chemical composition from pure ‘attraction’ nectars. If the
peristome nectar was mainly optimized for facilitating
water condensation, one might expect a smaller concen-
tration of (expensive) amino acids and a larger proportion
of (cheap) sugars.
Peristome nectar appears to play a less important role
in many other Nepenthes species. For example, we found
that the other variety of N. rafflesiana co-occurring in
Brunei, var. elongata, produces far less peristome nectar
(U. Bauer 2007, unpublished results). However, it
possesses slippery wax crystals on its inner pitcher walls
and therefore does not rely exclusively on ‘peristome
aquaplaning’ for prey capture. In contrast to the
‘aquaplaning’ mechanism, the efficiency of slippery wax
crystals is probably independent of weather conditions
and not temporally variable. Further comparative work is
needed to determine whether the possession of an
additional, wetness-independent capture mechanism
enables waxy Nepenthes species to colonize a broader
range of habitats than their congeners.
Specialized pitcher peristomes with strikingly similar
surface structures are found in several non-related genera
such as Nepenthes (Nepenthaceae), Cephalotus (Cephalo-
taceae) and Darlingtonia (Sarraceniaceae). Moreover, all
these plants possess nectaries located on the peristome
(Juniper et al. 1989). We conjecture that all these plants
not only possess a similar wetness-based capture
mechanism but also exhibit a temporally variable trapping
efficiency as reported in this study.
We acknowledge Konrad O¨chsner from the University of
Wu ¨rzburg for the technical development of the circuits used
for the measurements of peristome conductance. We would
like to thank Olusegun Osunkoya, Ulmar Grafe and David
Marshall from the University of Brunei Darussalam (UBD)
and the Brunei Forestry Department for kind permission
to conduct field research, and the Brunei Museum and
time of day
n = 61
proportion of ants (%)
15.30 16.3017.1518.05 18.5520.0001.30
n = 61
proportion of ants (%)
n = 77
proportion of ants (%)
Figure 5. Capture efficiency and peristome wetting measured
simultaneously on three N. rafflesiana var. typica pitchers from
the sameplant:(a) unmanipulated control, (b) intact nectaries,
peristome rinsed with water and (c) nectaries removed and
3 days before the start of the observations.
264U. Bauer et al.Harmless nectar source or deadly trap
Proc. R. Soc. B (2008)
Agriculture Department for permission to export specimens.
This study was funded by studentships from the DAAD and
Trinity College Cambridge to U.B., and by research grants of
the Cambridge Isaac Newton Trust and the DFG (SFB
567/C6 and Emmy-Noether Fellowship FE 547/1 to W.F.).
Barbosa, P. & Castellanos, I. (eds) 2005 Ecology of predator–
prey interactions, Oxford, UK: Oxford University Press.
Bohn, H. F. & Federle, W. 2004 Insect aquaplaning:
Nepenthes pitcher plants capture prey with the peristome,
a fully wettable water-lubricated anisotropic surface. Proc.
Natl Acad. Sci. USA 101, 14 138–14 143. (doi:10.1073/
Bradshaw, W. E. &Creelman, R. A.1984 Mutualism between
the carnivorous purple pitcher plant and its inhabitants.
Am. Midl. Nat. 112, 294–304. (doi:10.2307/2425436)
Browne, C. A. 1922 Moisture absortive power of different
sugars and carbohydrates under varying conditions of
atmospheric humidity. J. Ind. Eng. Chem. 14, 722.
Clarke, C. M. & Kitching, R. L. 1995 Swimming ants and
pitcher plants: a unique ant–plant interaction from
Borneo. J. Trop. Ecol. 11, 589–602.
Clarke, C. & Wong, K. M. 1997 Nepenthes of Borneo. Kota
Kinabalu, Malaysia: Natural History Publications.
Deppe, J. L., Dress, W. J., Nastase, A. J., Newell, S. J. &
from pitchers of Sarracenia purpurea L. with and without
insect visitors. Am. Midl. Nat. 144, 123–132. (doi:10.1674/
Driver, P. & Humphries, N. 1988 Protean behavior: the biology
of unpredictability. Oxford, UK: Oxford University Press.
Elias, T. S. 1983 Extrafloral nectaries: their structure and
distribution. In The biology of nectaries (eds B. L. Bentley &
T. S. Elias), pp. 174–203. New York, NY: Columbia
Ellison, A. M. & Gotelli, N. J. 2001 Evolutionary ecology of
carnivorous plants. Trends Ecol. Evol. 16, 623–629.
Gaume, L., Gorb, S. & Rowe, N. 2002 Function of epidermal
surfaces in the trapping efficiency of Nepenthes alata
Gorb, E., Haas, K., Henrich, A., Enders, S., Barbakadze, N.
& Gorb, S. 2005 Composite structure of the crystalline
epicuticular wax layer of the slippery zone in the pitchers
of the carnivorous plant Nepenthes alata and its effect on
insect attachment. J. Exp. Biol. 208, 4651–4662. (doi:10.
Herrera, C. M. & Pellmyr, O. (eds) 2002 Plant–animal
interactions: an evolutionary approach, Oxford, UK: Black-
well Science Ltd.
Ho ¨lldobler, B. & Wilson, E. O. 1990 The ants. Cambridge,
MA: Belknap Press.
Jebb, M. 1991 An account of Nepenthes in New Guinea. Sci.
New Guinea 17, 7–54.
Jebb, M. & Cheek, M. 1997 A skeletal revision of Nepenthes
(Nepenthaceae). Blumea 42, 1–106.
Juniper, B. E. & Burras, J. K. 1962 How pitcher plants trap
insects. New Sci. 13, 75–77.
Juniper, B. E., Robins, R. J. & Joel, D. M. 1989
The carnivorous plants. London, UK; San Diego, CA:
Klemm, O., Milford, C., Sutton, M., van Putten, E. &
Spindler, G. 2002 A climatology of leaf surface wetness.
Theor. Appl. Climatol. 71, 107–117. (doi:10.1007/s704-
Knoll, F. 1914 U¨ber die Ursache des Ausgleitens der
Jahr. Wiss. Bot. 54, 448–497.
Krebs, J. R. & Davies, N. B. 1997 Behavioural ecology: an
evolutionary approach. Oxford, UK: Blackwell.
Lloyd, F. E. 1942 The carnivorous plants. Chronica botanica,
vol. 9. New York, NY: Ronald Press.
Merbach, M. A., Zizka, G., Fiala, B., Maschwitz, U. &
Booth, W. E. 2001 Patterns of nectar secretion in five
Nepenthes species from Brunei Darussalam, Northwest
Borneo, and implications for ant–plant relationships. Flora
Merbach, M. A., Zizka, G., Fiala, B., Merbach, D., Booth,
W. E. & Maschwitz, U. 2007 Why a carnivorous plant
cooperates with an ant—selective defense against pitcher-
destroying weevils in the myrmecophytic pitcher plant
Nepenthes bicalcarata Hook. F. Ecotropica 13, 45–56.
Moran, J. A. 1996 Pitcher dimorphism, prey composition and
the mechanisms of prey attraction in the pitcher plant
Nepenthes rafflesiana in Borneo. J. Ecol. 84, 515–525.
Moran, J. A., Booth, W. E. & Charles, J. K. 1999 Aspects of
pitcher morphology and spectral characteristics of six
bornean Nepenthes pitcher plant species: implications for
prey capture. Ann. Bot. 83, 521–528. (doi:10.1006/anbo.
Owen, T. P. & Lennon, K. A. 1999 Structure and
development of the pitchers from the carnivorous plant
Ratsirarson, J. & Silander, J. A. 1996 Structure and
dynamics in Nepenthes madagascariensis pitcher plant
micro-communities. Biotropica 28, 218–227. (doi:10.
Stowe, M. K., Tumlinson, J. H. & Robert, R. H. 1987
Chemical mimicry: bolas spiders emit components of
moth prey species sex pheromones. Science 236, 964–967.
Tan, H. T. W. (ed.) 1997 A guide to the carnivorous plants of
Singapore, Singapore: Singapore Science Centre.
Wa ¨ckers, F. L., van Rijn, P. C. J. & Bruin, J. (eds) 2005 Plant-
provided food for carnivorous insects: protective mutualism and
its applications, Cambridge, UK: Cambridge University
Harmless nectar source or deadly trap
U. Bauer et al.
Proc. R. Soc. B (2008)