Journal of Tropical Ecology (2012) 28:97–104. © Cambridge University Press 2011
Cross-habitat predation in Nepenthes gracilis: the red crab spider
Misumenops nepenthicola inﬂuences abundance of pitcher dipteran larvae
Trina Jie Ling Chua
and Matthew Lek Min Lim
Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543
† Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138, USA
(Accepted 22 October 2011)
Abstract: Phytotelmata (plant-held waters) are useful ecological models for studying predator–prey interactions.
However, the ability of terrestrial predators to inﬂuence organism abundance within phytotelmata remains poorly
studied. We investigated the predation of two pitcher-dwelling spiders, the red crab spider Misumenops nepenthicola and
the yellow crab spider Thomisus nepenthiphilus (Araneae: Thomisidae) on dipteran larval abundance by manipulating
their presence in the pitcher Nepenthes gracilis. Lower abundance in the larvae of the mosquito Tripteriodes spp. and
increased spider mass were recorded after M. nepenthicola was introduced into laboratory-maintained pitchers (n = 10);
T. nepenthiphilus did not affect larval abundance and a decrease in spider mass was recorded. Further investigations
on two other dipteran larval species, the scuttle ﬂy Endonepenthia schuitemakeri and gall midges Lestodiplosis spp.,
reported reduced numbers with the introduction of M. nepenthicola. We further tested this predation on dipteran larval
abundance by its introduction, removal, and re-introduction to pitchers in the ﬁeld (n = 42) over 1 mo. The spider’s
absence and presence signiﬁcantly inﬂuenced larval numbers: all four dipteran species reported a signiﬁcant decrease
in numbers after M. nepenthicola was introduced. These results are one of the ﬁrst to demonstrate the inﬂuence of a
terrestrial phytotelm forager on the abundance of pitcher organisms via direct predation, reiterating the ecological
importance of terrestrial phytotelm predators on phytotelm community structure and dynamics.
Key Words: crab spiders, Culex, Endonepenthia schuitemakeri, Lestodiplosis, Misumenops nepenthicola, Nepenthes gracilis,
phytotelmata, predation, Thomisus nepenthiphilus, Tripteriodes
Natural microcosms offer opportunities for an array of
ecological studies, such as the role of predation in biotic
interactions, shaping food webs and altering community
structure and ecosystem functions. Phytotelmata (plant-
held waters; Kitching 2001) are popular study models of
arthropod–plant mutualism food webs and community
structure (Armbruster et al. 2002, Clarke et al. 2009,
Kitching 2001, Maguire et al. 1968, Moon et al. 2010,
Peterson et al. 2008), focusing on the apex predators
that reside within the same aquatic habitat as their prey.
However, there has been recent interest in the cross-
habitat (i.e. terrestrial to aquatic) predatory effects of
terrestrial inhabitants (Romero & Srivastava 2010).
Phytotelm communities have been the focus of
numerous studies of community dynamics for the past
three decades (Kitching 2000, Maguire et al. 1968,
Corresponding author. Email: firstname.lastname@example.org
Mogi & Chan 1997, Mogi & Yong 1992, Mouquet et al.
2008, Naeem 1988, Seifert & Seifert 1976). Amongst
these, pitchers are unique as these highly modiﬁed leaf
structures, holding a digestive ﬂuid, lure, trap and kill any
organism that falls into these pitfalls. These vessels possess
several key traits that facilitate their heterotrophism:
chemical and colour cues that attract prey (Bennett &
Ellison 2009, Jurgens et al. 2009, Schaefer & Ruxton
2008), slippery inner wall surfaces (Gorb et al. 2004,
Scholz et al. 2010), and a highly viscous (Di Giusto et al.
2008), acidic and hypoxic ﬂuid (due to decomposing
insects). Collectively, these factors constitute a hostile
environment and pose a challenge for any organisms.
Rather, numerous organisms have adapted to living,
many exclusively, within pitchers as nepenthebionts (i.e.
obligate Nepenthes pitcher dwellers), holding positions
as apex predators, mesopredators a nd scavengers that
regulate top-down and bottom-up forces (Kneitel & Miller
2002). In comparison, little is known about the ecological
importance of terrestrial phytotelm organisms (Greeney
98 TRINA JIE LING CHUA AND MATTHEW LEK MIN LIM
Figure 1. Food web of a Nepenthes gracilis pitcher (modiﬁed from Clarke
& Kitching 1993, Phillipps et al. 2008, Tan 1997) organized in trophic
levels. Arrows in bold indicate predator–prey interactions involved in
Although many terrestrial phytotelm inhabitants
are known (for a review see Greeney 2001), those
that forage across terrestrial–aquatic environments are
seldom recorded. Clarke & Kitching (1995) probably
provided the ﬁrst empirical evidence of cross-habitat
predation in the golden ant Camponotus schmitzi
and its host plant Nepenthes bicalcarata, where the
ant signiﬁcantly inﬂuenced the abundance of ﬁlter-
feeding mosquito larvae. The nepenthebiont crab spiders
(Araneae: Thomisidae) are the only other group of
organisms documented to forage into Nepenthes pitcher
ﬂuid (Barthlott et al. 2007, Clarke 1997, 2001; Phillipps
et al. 2008, Pollard 2005; Figure 1) for live dipteran larvae
(Clarke 1998, Moran 1993). These larvae are Nepenthes
obligates and assume key roles within the food web
(Figure 1); however, nothing is known about t he aquatic
foraging ability of the terrestrial crab spiders and their
potential to alter dipteran larval abundance.
Here we investigate the nepenthebiont crab spiders’
foraging ability to alter the aquatic larval abundance
of the tropical pitcher plant Nepenthes gracilis.We
hypothesize that the crab spiders’ presence signiﬁcantly
affects the abundance of nepenthebiont dipteran larvae
species in N. gracilis. As pitchers provide natural
microcosms amenable to both laboratory and ﬁeld
experiments (Srivastava et al. 2004), we conducted
laboratory-based studies to investigate the aquatic
foraging behaviour of the crab spiders by introducing one
individual into one pitcher containing any of the three
dipteran larvae species; a reduction in larval abundance,
coupled with weight increase in the spider will verify this
ability. Field experiments then determined the spiders’
inﬂuence on the abundance of these aquatic dipteran
larvae. A signiﬁcant decrease in larval abundance in the
presence of the crab spiders will suggest the ecological
importance of these predators, with probable implications
for the Nepenthes food web, and highlight the importance
of the ecological roles of terrestrial animals with aquatic
predatory traits within phytotelmata.
Nepenthes gracilis Korth. (Figure 2a) is widespread in
Singapore, its pitchers home to a diverse macrofauna
dominated by insects (Kitching 2001). Larvae of several
dipteran species (mosquitoes Tripteriodes spp. and Culex
spp., scuttle ﬂy Endonepenthia schuitemakeri (Schmitz,
1932) and gall midge Lestodiplosis spp. (Figure 2d–g))
occupy the various trophic zones within these pitchers
(Figure 1). Residing within pitchers and above the
ﬂuid are two species of thomsids; the red crab spider
Misumenops nepenthicola (Pocock, 1898) (Figure 2b) and
the yellow crab spider Thomisus nepenthiphilus (Fage,
1930) (Figure 2c). Only the foraging of M. nepenthicola,
but not Thomisus nepenthiphilus, has been recorded within
N. gracilis (Kitching 2000).
We investigated the foraging behaviour of Misumenops
nepenthicola and Thomisus nepenthiphilus on dipteran
larvae that dwell within Nepenthes pitchers using 10 adult
females (M. nepenthicola; body length (mean ± SD): 5.4 ±
0.5 mm, T
. nepenthiphilus; body length: 7.3 ± 0.5 mm)
and 200 mosquito larvae (Tripteriodes spp.; body length:
approximately 4 mm), all collected from Kent Ridge Park,
a secondary forest in Singapore. Pitcher ﬂuid (collected
from 20 pitchers) was ﬁltered to remove detritus and live
organisms. We also purchased N. gracilis from a local
nursery; these were maintained in clear plastic tanks
(39 × 24.5 × 30 cm). Twenty fresh pitchers (mean ±
SD: height: 7.30 ± 1.65 cm; width: 1.50 ± 0.28 cm)
were selected, each rinsed thoroughly (using distilled
water from a squirt bottle) prior to the experiment.
Pitcher contents were discarded, and the ﬂuid replaced
Cross-habitat predation inﬂuences pitcher inhabitants 99
Figure 2. Organisms involved in this study: a freshly opened Nepenthes gracilis pitcher (a), red crab spider Misumenops nepenthicola (b), yellow crab
spider Thomisus nepenthiphilus (c), mosquito larvae Tripteriodes spp. (d) and Culex spp. (e), scuttle ﬂy larva Endonepenthia schuitemakeri (f), and gall
midge larva Lestodiplosis spp. (g). Scale bar represents 1 cm (a, b, c) and 1 mm (d, e, f, g).
by those collected in the ﬁeld (2 ml of ﬂuid per pitcher)
prior to experiment. Two circular plastic containers (4.3
cm diameter × 11.2 cm height) ensured containment
of an individual spider in each pitcher. Experiment
was limited to 5 d because many N. gracilis had
withered and most mosquito larvae had moulted into
pupae and emerged as adults in earlier trials that
lasted 1 wk. We accounted for the number of larvae
(10 Tripteroides spp.) on days 1 and 3 to check for
cannibalism. The mass of each crab spider (to the nearest
0.00001 g) was recorded after collection (i.e. day 1)
from Kent Ridge Park, prior to their introduction into
the pitchers and maintained on sugar solution ad libitum
via dental roll soaked in diluted sugar solution till day 3.
100 TRINA JIE LING CHUA AND MATTHEW LEK MIN LIM
Figure 3. Summary of ﬁeld-based experiment depicting the periods of colonization, presence and absence of crab spiders, and sequence of data
collection and pitcher manipulation (i.e. introduction and removal of spider).
On day 5, we took note of larvae carcases (i.e. dead larvae
not eaten by the spider) to ensure that all larvae were
We repeated the above procedure but used two dipteran
larvae species in separate trials: the carrion-feeding
scuttle ﬂy larva E. schuitemakeri (length: 0.4 cm) and
the predatory gall midge larva Lestodiplosis spp. (length:
0.2 cm). Only ﬁve individuals of each species were
used due to their lower abundance observed in the ﬁeld
(pers. obs.). We excluded T. nepenthiphilus from this and
further experiments because it did not forage on aquatic
mosquito larvae. All experimental animals, plants and
units were maintained in a laboratory under controlled
environmental conditions (relative humidity 80–85%;
C ± 1
C; light regime 12:12 h; lights o n
at 0800 h).
We investigated the relationship between M. nepenthicola
and the abundance of phytotelm dipteran larvae in
natural occurring populations of N. gracilis at Kent Ridge
Park, Singapore. As M. nepenthicola abandoned shorter
pitchers (pers. obs.), we only used pitchers more than
6 cm high and unopened at time of selection. From
two separate experimental periods (22 October 2009–3
December 2009; 24 December 2009–4 February 2010),
we tagged a total of 65 unopened N. gracilis. These
were surveyed twice a week from the time they opened
to the time they withered or until the end of the ﬁeld
experiment, whichever came ﬁrst. We also introduced
a 2-wk colonization period to allow establishment of
secondary consumers and scavengers, as freshly opened
pitchers harboured neither aquatic dipteran larvae nor
crab spiders (pers. obs.).
Field experiments commenced 2 wk after the pitchers
had opened (Figure 3); a small number of p itchers that
harboured spiders were excluded from our data. Contents
of qualiﬁed pitchers were emptied into individual collec-
tion vials and pitchers rinsed with water via a squirt bottle
into a second vial to remove residual contents. Both vials
were then transported to a laboratory and the live aquatic
dipteran larvae identiﬁed (based on morphospecies) and
counted under a stereomicroscope. We returned all
dipteran larvae and contents to their respective pitchers
on the same day, and introduced one female adult M.
nepenthicola (0.50 ± 0.10 cm) into each pitcher for 1
wk. We repeated the above procedure (i.e. counting of
larvae and returning contents to the respective pitcher)
two more times; with the resident crab spider ﬁrst
removedandmaintainedin thelaboratory (sugarsolution
provided ad libitum) and ﬁnally reintroduced to the same
pitcher (Figure 3). We used 7 d per treatment (i.e. spider
absent/present) because laboratory experiments revealed
that many M. nepenthicola had consumed most of their
prey within 2 d. Introduction, removal and subsequent
re-introduction of M. nepenthicola into pitchers over 4 wk
enabled the realistic testing of this spider as a predator
along with other concurrent activities (e.g. egg-laying by
dipteran adults, newly hatched or moulted aquatic dip-
teran larvae, newly emerged dipteran adults from pupae,
other predation and parasitic activities, and changes to
pitcher detritus) that can affect larval abundance.
Cross-habitat predation inﬂuences pitcher inhabitants 101
We inspected all pitchers for spiders every 3–4 d to
ensure its status (i.e. spider present or absent). If we
found a spider in a pitcher designated as ‘spider absent’,
the pitcher ﬂuid and its contents were ﬁrst collected
before the pitcher was ﬁlled with distilled water to
the brim so that removal, only if the spider surfaced
at the mouth of the pitcher upon depletion of its air
supply, was easy. This approach is necessary as, upon
disturbance, M. nepenthicola never fails to drop into
the ﬂuid and stays at the bottom of the pitcher until
its air supply (i.e. air bubble entrapped in a small pit
on the abdomen ventral side) is depleted after several
minutes. Pitcher contents were returned after the spider
was removed. We also reintroduced M. nepenthicola into
pitchers that were supposed to hold a spider but were
otherwise absent; a spider usually climbed on and into a
pitcher within a few minutes. We assumed that these
newly introduced adult female crab spiders, collected
from Kent Ridge Park on the same day, have similar
satiation levels to other conspeciﬁcs in experimental
pitchers. We attached a pair of Velcro
smeared with Singer
Oil twice a week) on each
pitcher’s leaf blade to dissuade experimental spiders from
leaving their designated pitchers and non-experimental
crab spiders from entering experimental pitchers. We
also excluded, from data analyses, a small number
of pitchers with withered lids and/or contained egg
We compared the larval abundance, in the absence
and presence of spiders, of the same pitcher using a
related sampling approach, the Friedman test (PASW
Statistics, version 18; signiﬁcance level at 0.05) and a
non-parametric pairwise comparison (Siegel & Castellan
1988) for multiple group comparisons of related samples.
We only considered pairwise comparisons when the
corresponding Friedman test was signiﬁcant (i.e. absolute
difference value exceeds the corresponding critical
difference, denoting a signiﬁcant difference for that
respective pair; Siegel & Castellan 1988). We only
report relevant pairwise comparisons of interest to our
We adopted a related-sampling approach owing to the
limited abundance and occurrences of M. nepenthicola
within pitchers from only one site in Singapore (i.e. Kent
Ridge Park). Each pitcher was used as its own control
to minimize any potential confounding variables. We
sought to minimize the possibility of temporal effects by
(1) repeating the procedure of spider introduction one
more time for each pitcher, and (2) carrying out the entire
experimental procedure on two separate occasions.
The weight of M. nepenthicola increased signiﬁcantly
on day 5 (χ
= 15.8, df = 2, P < 0.001; Figure 4a)
after removal from experimental pitchers. The mean
larval abundance of Tripteroides spp. reduced signiﬁcantly
after M. nepenthicola was introduced on the third day
= 20.0, df = 2, P < 0.001; Figure 4b). There was
no change in larval abundance of Tripteroides spp.
when Thomisus nepenthiphilus was introduced (Figure
4b) and a signiﬁcant decrease in predator weight was
= 20.0, df = 2, P < 0.001; Figure 4a).
Hence, T. nepenthiphilus was excluded from further ﬁeld
manipulative experiments as it did not feed on mosquito
Signiﬁcant reductions in the larval abundance of E.
= 15.0, df = 2, P < 0.001; Figure 4d)
andLestodiplosis spp. (χ
= 16.8,df = 2,P < 0.001;Figure
4f) were observed after M. nepenthicola was introduced.
Although M. nepenthicola had signiﬁcant weight changes
throughout the experiment (feeding on E. schuitemakeri:
= 18.6, df = 2, P < 0.001 (Figure 4c); feeding on
Lestodiplosis spp.: χ
= 18.7, df = 2, P < 0.001 (Figure
4e)), a signiﬁcant mass increment after the spider’s
introduction was only observed when feeding on E.
schuitemakeri (Figure 4c).
A total of 42 pitchers were involved in statistical
analyses. Over 4 wk (i.e. wk 3 to 6), dipteran larval
abundance signiﬁcantly changed when M. nepenthicola
was introduced or removed (Tripteroides spp.: χ
df = 3, P < 0.001; Culex spp.: χ
= 19.0, df = 3, P < 0.001;
E. schuitemakeri: χ
= 33.7, df = 3, P < 0.001; Lestodiplosis
= 24.2, df = 3, P < 0.001), with a general
decrease in prey abundance in the spider’s presence
and concomitant increase after the spider’s removal
Our study is one of the ﬁrst to demonstrate the
inﬂuence of a terrestrial phytotelm forager on key
phytotelm organisms via direct predation: Misumenops
nepenthicola, but not T. nepenthiphilus, signiﬁcantly
inﬂuences phytotelm dipteran larval abundance in N.
gracilis. This supports the ecological importance of cross-
habitat-capable predators in inﬂuencing phytotelm insect
larvae numbers (Greeney 2001, Romero & Srivastava
102 TRINA JIE LING CHUA AND MATTHEW LEK MIN LIM
Figure 4. Effects of spider’s absence and p resence on dipteran larval abundance and spider’s corresponding weight. Effects of absence (days 1 and
3) and presence (day 5) of the red crab spider Misumenops nepenthicola (ﬁlled circles) and the y ellow crab spider Thomisus nepenthiphilus (unﬁlled
circles) and their corresponding weight (median) (a) relating to the abundance of the mosquito larvae Tripteroides spp. (b). Effects of absence (days
1 and 3) and presence (day 5) of M. nepenthicola and its corresponding weight (median) (c, e) relating to the abundance of the larvae of the
scuttle ﬂy Endonepenthia schuitemakeri (squares) (d) and gall midge Lestodiplosis spp. (triangles) (f). All spiders were introduced on day 3 only after
experimental larval abundances were recorded for that day. For all data, n = 10 replicates. Different letters represent signiﬁcant difference within
experiments/species at P < 0.001, applying post hoc Friedman test.
Figure 5. Box-plots on predation of Misumenops nepenthicola on dipteran
larvae. Effects of absence (wk 3 and 5) and presence (wk 4 and
6) of M. nepenthicola (presence indicated by spider inserts) on larval
abundance of mosquitoes Culex spp. (a) and Tripteriodes spp. (b), scuttle
ﬂy Endonepenthia schuitemakeri (c) and gall midge Lestodiplosis spp. (d).
Central bar: median; hinges: 25 and 75%; whiskers: 5 and 95%. For all
data, n = 42 replicates. Different letters represent signiﬁcant difference
within species at P < 0.001, applying post hoc Friedman test.
2010), suggesting this spider’s role in regulating larval
abundance in N. gracilis.
Evidence of aquatic dipteran larval predation
The decrease in mosquito larval abundance and increase
in spider mass reported here support earlier claims on
the aquatic foraging capability of M. nepenthicola (Clarke
1998, Moran 1993). A small pit on the ventral abdomen
of M. nepenthicola allows storage of a small reserve
supply of air that facilitates aquatic foraging and possibly
predator avoidance. Like all crab spiders, M. nepenthicola
possesses eyes that provide excellent spatial resolution
(Land 1985). Its relatively longer legs possibly allow
swift and safe locomotion into and out of the pitcher
ﬂuid since the pitcher inner wall is usually lined with
numerous draglines. In contrast, T. nepenthiphilus did not
affect mosquito larval abundance; a signiﬁcant weight
decline meant it is not capable of aquatic foraging. No
cannibalism in mosquito larvae was recorded, since their
numbers did not differ after 3 and 5 d during laboratory
experiments. Although the aquatic foraging ability of M.
nepenthicola is further established with lower abundances
of E. schuitemakeri and Lestodiplosis spp. larvae after its
introduction, results of the latter’s abundance did not
concur with spider weight change: spiders lost weight
with decreased Lestodiplosis spp. abundances. We believe
that the total amount of Lestodiplosis biomass consumed
was inadequate to sustain an increase in spider mass,
Cross-habitat predation inﬂuences pitcher inhabitants 103
given that they are half the size (2 mm) of E. schuitemakeri
and Tripteroides (both 4 mm).
Though M. nepenthicola is described as a nepenthebiont,
empirical data supporting its symbiotic relation with N.
gracilis is lacking. Clarke (1997) proposed that the entire
in-fauna of Nepenthes pitchers is in a symbiotic interaction
with the plant as these organisms contribute to the more
efﬁcient breakdown of prey items within the pitchers.
Additionally, Phillipps et al. (2008) explained that while
M. nepenthicola feeds on insects, the plant may beneﬁt
from the spider’s waste products, suggesting this spider’s
symbiotic interaction with N. gracilis (also see Clarke et al.
2009, Romero et al. 2006). In the mutualistic interaction
between the ant C. schmitzi and its host pitcher plant, N.
bicalcarata, Clarke & Kitching (1995) reported that, while
providing this ant with a domicile within the swollen
tendrils of the pitchers, the host in fact beneﬁts from the
comminution of larger prey items by the ants, which the
plant extracts from the pitcher ﬂuid. Without this ant-
assisted breakdown, the pitcher will likely become anoxic
as the rate of decay outruns that of digestion (Clarke
& Kitching 1995). Also, these ants prey on organisms
within the pitcher, possibly acting as a top predator within
the contained food web (Kitching 2001). Likewise, by
regulating the abundance of dipteran larvae in the pitcher
ﬂuid via direct predation, M. nepenthicola can reduce the
potential amount of prey putrefaction in N. gracilis that
can disrupt the plant’s digestive system.
The predation of M. nepenthicola on various dipteran
species suggests that it can regulate dipteran larval
populations and indirectly affect the food chain and
ecosystem within pitchers. Several well-studied food webs
of N. gracilis (Clarke & Kitching 1993, Phillipps et al. 2008,
Tan 1997) have proposed M. nepenthicola as a higher
trophic level consumer and possibly an apex predator in
pitcher phytotelmata (Figure 1). Our results support this
possibility: M. nepenthicola can inﬂuence t he population of
key organisms in N. gracilis. Future research should focus
on this spider’s potential to alter food web and community
structure (e.g. altering the balance between aquatic
detritivores and predators) and the ecosystem functions
these dipteran larvae provide. We also propose that future
ecological studies of phytotelm communities include in-
vestigating the potential of terrestrial phytotelm dwellers,
particularly those with aquatic foraging ability, to inﬂu-
ence the aquatic organisms’ populations and hence food
web and ecosystem functions. Finally, with global warm-
ing altering predator–prey interactions (Traill et al. 2010),
we urge that future phytotelm dipteran studies should
take into consideration the effect of abiotic factors, in
particular temperature (Hoekman 2010), in inﬂuencing
pitcher community structure and ecosystem function.
We thank National Parks Board Singapore for their
permission to carry out this research under permit
number NP/RP950. We also wish to express our
appreciation to Charles Clarke for his help in the
identiﬁcation of mosquito larvae, and Wan Jean Lee and
Tien Ming Lee for their comments and suggestions on the
manuscript. This project was supported ﬁnancially by a
ﬁnal-year project grant from the National University of
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