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Cross-habitat predation in Nepenthes gracilis: The red crab spider Misumenops nepenthicola influences abundance of pitcher dipteran larvae

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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.
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Journal of Tropical Ecology (2012) 28:97–104. © Cambridge University Press 2011
doi:10.1017/S0266467411000629
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
,,1
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
INTRODUCTION
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,
1
Corresponding author. Email: matthewlim@oeb.harvard.edu
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
2001).
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
this study.
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.
METHODS
Study species
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).
Laboratory experiments
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
accounted for.
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%;
temperature 25
C ± 1
C; light regime 12:12 h; lights o n
at 0800 h).
Field experiments
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
R
fasteners (lightly
smeared with Singer
R
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
sacs.
Statistical analysis
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
hypotheses.
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.
RESULTS
Laboratory experiments
The weight of M. nepenthicola increased significantly
on day 5 (χ
2
= 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
(χ
2
= 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
observed (χ
2
= 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
larvae.
Significant reductions in the larval abundance of E.
schuitemakeri (χ
2
= 15.0, df = 2, P < 0.001; Figure 4d)
andLestodiplosis spp. (χ
2
= 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:
χ
2
= 18.6, df = 2, P < 0.001 (Figure 4c); feeding on
Lestodiplosis spp.: χ
2
= 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).
Field experiments
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
2
= 20.7,
df = 3, P < 0.001; Culex spp.: χ
2
= 19.0, df = 3, P < 0.001;
E. schuitemakeri: χ
2
= 33.7, df = 3, P < 0.001; Lestodiplosis
spp.: χ
2
= 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
(Figure 5).
DISCUSSION
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).
Future directions
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.
ACKNOWLEDGEMENTS
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
Singapore.
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... Differentiating the Dasyhelea species can be difficult, and many studies (e.g., Bittleston et al., 2016;Gaume et al., 2019; considered the abundance of the whole genus without noting the associations of each species with specific Nepenthes hosts. This taxon is most commonly recorded from the pitchers of Nepenthes ampullaria, but also occur, albeit less frequently, in the pitchers of Nepenthes gracilis and Nepenthes rafflesiana Mogi & Chan, 1997;Chua & Lim, 2012;. However, the degree to which the different Dasyhelea species specialise in one or more Nepenthes host species is unclear, as various published studies have reported different associations and association strengths (Wirth & Beaver, 1979;Mogi & Chan, 1997;Lam et al., in press). ...
... Lestodiplosis species larvae are common inhabitants of Nepenthes gracilis pitchers (Choo et al., 1997;Chua & Lim, 2012;Gaume et al., 2019), where multiple individuals are known to collectively attack and feed on inquiline Dasyhelea species larvae (Mogi & Chan, 1996). However, it is unlikely that Dasyhelea species are the only food resource of Lestodiplosis species, since both taxa do not appear to co-occur in sufficient frequencies in situ for one to be completely reliant on the other as a prey resource (Gaume et al., 2019;WNL, unpublished data). ...
... The crab spiders (Thomisidae, Araneae). -Two crab spider species (Thomisidae) are known to inhabit the pitchers of Nepenthes gracilis locally-Thomisus nepenthiphilus (Fig. 6.22) and Misumenops nepenthicola (Fig. 6.23) (Choo et al., 1997;Mogi & Chan, 1997;Chua & Lim, 2012). Both species are also regularly found in pitchers of Nepenthes rafflesiana in Borneo , although this is only very rarely observed in Singapore (Choo et al., 1997;WNL, pers. ...
... Crab spiders (Thomisidae) are known to inhabit the pitchers of several Nepenthes species (Clarke 2001;Rembold et al. 2012). Misumenops nepenthicola is among the best studied of these crab spiders, and is known to prey on aquatic dipteran larvae (Chua and Lim 2012), and, anecdotally, emerging adult dipteran inquilines and other pitcher visitors (Clarke 2001). This species and Thomisus nepenthiphilus are known to inhabit pitchers of N. gracilis in Singapore, and are completely dependent on the plant for their survival (Choo et al. 1997). ...
... However, small prey items may yield lower benefit to pitchers after they are consumed by crab spiders. M. nepenthicola thus appears to have a larger dietary breadth which also includes aquatic dipteran larvae (Chua and Lim 2012) and emerging dipteran inquilines (Clarke 2001), while being less adapted to ambushing large flying pitcher visitors, on which T. nepenthiphilus may specialize. ...
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Positive species interactions are ubiquitous and crucial components of communities, but they are still not well incorporated into established ecological theories. The definitions of facilitation and mutualism overlap, and both are often context dependent. Many interactions that are facilitative under stressful conditions become competitive under more benign ones. This is known as the stress-gradient hypothesis, which is a specific case of context dependency. Stress can be further divided into resource and non-resource categories, but a better mechanistic understanding is necessary to improve the theory’s predictions. We examined if two pitcher-dwelling crab spiders (Thomisidae), Thomisus nepenthiphilus and Misumenops nepenthicola, can facilitate nitrogen sequestration in their pitcher plant host, Nepenthes gracilis, by ambushing pitcher-visiting flies and dropping their carcasses into pitchers after consumption. This relationship is, by definition, both mutualistic and facilitative. Laboratory experiments found that both crab spiders increased prey-capture rates of N. gracilis. Nutrient analyses showed that both crab spiders also decreased per unit nitrogen yield of prey. Using experiment duration as a proxy of prey-resource availability, we constructed a mechanistic conceptual model of nutritional benefit. The nutritional benefit received by N. gracilis from T. nepenthiphilus decreases with increasing levels of the limiting resource in the environment (i.e., decreasing levels of resource stress). Our findings suggest that any nutritional mutualism that increases the quantity of resource capture (e.g. number of prey individuals) but decreases the quality of the captured resource (e.g. nitrogen content of individual prey) will necessarily conform to the resource-based predictions of the stress gradient hypothesis.
... Moreover, the results of present study showed that during samples collection red crab spiders, Misumenops nepenthicola, existed and constructed their nests on surface wall inside pitchers. The observation of Chua and Lim (2012) supported that Misumenops nepenthicola were predators of Tripteroides spp. and density mosquito larvae decreased dramatically in pitchers where the red crab spiders were present. ...
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This study examined the abundance of various immature mosquito species and ascertained selected environmental conditions in the pitcher. A total of hundred pitchers (Nepenthes mirabilis var. mirabilis), including 50 upper pitchers and 50 lower pitchers, were collected during rainy and dry seasons from Songkhla Province, Thailand. A total of 546 mosquito larvae belonging to two genera and three species were identified. Among the collections, 526 larvae of Tripteroides tenax (96.34%), followed by 11 larvae of Tripteroides sp.1 (2.01%), and nine larvae of Toxorhynchites albipes (1.65%) were identified. The abundance of mosquito larvae was noted to be higher during rainy season than during dry season. Mosquito larvae abundance positively correlated with pitcher size, amount of detritus present, pH of the medium, abundance of microorganisms, and amount of total fluid present in pitchers. Variation in abundance of mosquito larvae existing in pitchers is influenced by the presence of predators therein and different seasons.
... Water pools formed by rainwater accumulation in the rosette's leaf axils (i.e. phytotelmata) provide valuable moist shelters where organisms can escape from desiccation, reproduce, and forage (Chua & Lim, 2012;Hénaut et al., 2018). Predators, like spiders, greatly benefit from the complex structure formed by rosettes and can access both aquatic and terrestrial prey (Barth et al., 1988b;Dias & Brescovit, 2003;Romero & Vasconcellos-Neto, 2005b). ...
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• Rosette‐shaped plants can amplify the diversity of predator arthropods and act as potential shelters for these animals in grassland ecosystems under grazing effect. • Here we evaluated the contribution of a vertical rosette‐shaped plant (Eryngium horridum) to patterns of spider diversity and functional traits in subtropical grasslands under different grazing intensities. We used a common sub‐shrub (Baccharis crispa) and the herbaceous vegetation as reference microhabitats. • Sampling was conducted in 23 plots described according to grazing intensity based on environmental co‐variables. Spiders were sampled with D‐Vac suction within patches of E. horridum, B. crispa, and the herbaceous vegetation. • Compared to the reference microhabitats, E. horridum harboured distinct community composition with a subset of exclusive species, and morphologically adapted spiders. • Spider richness increased in Eryngium plants as grazing pressure increased and the grassland became more simplified. Abundance of runners and space web‐builders responded in a similar fashion, while orb‐web builders were more abundant in E. horridum regardless of grazing intensity. • Our results indicate that these rosette plants positively affect top invertebrate predators, with a special role for sites with high grazing intensities where it promotes microhabitat complexity and aggregates more individuals and species. Thus, grassland management that alter Eryngium's occurrence must be conducted cautiously.
... This is in line with our observations that spiders routinely retrieved freshly captured prey from the pitcher fluid. Chua and Lim (2012) suggested that spiders feed primarily on aquatic infauna organisms; however, we rarely observed spiders hunting for live prey such as mosquito larvae in the pitcher fluid. Recent studies point toward a neutral or even mutualistic relationship because they observed spiders ambushing pitcher visitors and dropping the carcasses into the pitcher after feeding, thereby potentially increasing the prey intake of the plant (Lam & Tan, 2019;Lim, Lam, & Tan, 2018). ...
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Pitcher plants are flagship species for conservation and nature education alike. The diversity of interactions with animals beyond the plants' prey in particular captures people's imagination and ignites their interest and love for the natural world. Here we present observations and experimental data on the biology and behaviour of the pitcher‐inhabiting crab spider, Misumenops nepenthicola.
... Interspecific interactions clearly shape the inquiline communities within Nepenthes phytotelmata (Clarke & Kitching, 1993;Kitching, 2001). The diversity of such interactions, ranging from facilitation (Bradshaw & Creelman, 1984;Lam et al., 2017) to competition (Leong et al., 2018) and predation (Mogi & Chan, 1996;Chua & Lim, 2012;Lam et al., 2018a), make inquiline communities potentially valuable model systems for the study of community ecology and biodiversity phenomena (Srivastava et al., 2004). Nevertheless, knowledge gaps in the basic ecology and life history of some inquiline species greatly limit such a potential utility. ...
Article
Pitcher plants of the genus Nepenthes trap and digest invertebrate prey to supplement their nutrient requirements using fluid‐containing, modified leaves known as ‘pitchers’. Pitchers are habitats to many aquatic metazoan and microbial species known as ‘inquilines’. Mites (Histiostomatidae) are a common but poorly studied inquiline taxon – little is known of their life cycles and their interactions with other inquiline taxa. The objectives of this study were to (1) investigate interspecific interactions between inquiline Creutzeria mites, microbes and Endonepenthia schuitemakeri (Diptera: Phoridae) (2) quantify the net nutritional benefit of Creutzeria mites and other inquilines on Nepenthes gracilis nitrogen sequestration and (3) determine if E. schuitemakeri can act as dispersal agents for Creutzeria mites. In the first part of the study, Creutzeria mites were reared in vitro under simulated pitcher conditions for varying lengths of time. Their populations were found to increase exponentially with time, peaking 24.2 days into the experiment and decreasing thereafter. In the second experiment, in vitro experiments were established with different combinations of E. schuitemakeri larvae, ant prey biomass, ant prey species and Creutzeria mite addition. Mite population, fluid microbe density and total pitcher‐available nitrogen were measured at the end of 24 days as determined in the first part of the study. Confirmatory path analyses suggested that Creutzeria mites competed with microbes for prey resources (negative effect of microbe density on mite population) were not facilitated by E. schuitemakeri (no effect of E. schuitemakeri on mite population) and had a neutral to negative effect on pitcher nutrient sequestration (weak negative effect of mite population on pitcher‐available nitrogen). However, Creutzeria deutonymphs could not be found on any of the E. schuitemakeri adults emerged during the experiments, suggesting these utilize other inquiline species as dispersal agents, or require environmental/stress trigger factors to form deutonymphs. Pitcher plants of the genus Nepenthes trap and digest invertebrate prey to supplement their nutrient requirements using fluid‐containing, modified leaves known as ‘pitchers’. Pitchers are habitats to many aquatic metazoan and microbial species known as ‘inquilines’. In vitro experiments were used to examine the relationships between ubiquitous but poorly studied Creutzeria mites and their pitcher plant host, and with other pitcher inhabitants. Creutzeria mites were found to have a negligible effect on pitcher nutrient availability and appeared to compete with fluid microbes for prey resources. Creutzeria mites are likely to depend on other inhabitants as dispersal agents, but we did not find any evidence for their utilization of emerging scuttle fly adults for this purpose.
... This behaviour is believed to be a defensive adaptation against predatory birds or wasps (Pocock, 1898). Aside from the study of Lim et al. (2018) which showed that both crab spider species attack flesh flies (Chua & Lim, 2012;Clarke, 2001), has been observed attacking pitcher visitors (Clarke, 2001;Pocock, 1898) and has been filmed consuming recently drowned pitcher prey (an Oecophylla smaragdina ant worker; Planet Earth Episode 8: "Jungles" (2006), British Broadcasting Corporation). Reiskind (1978) also observed M. nepenthicola attacking struggling insect prey from the surface of pitcher fluids in N. rafflesiana and interpreted this to be a form of kleptoparasitism. ...
Article
1.Nutritional mutualisms are one of three major categories of mutualisms, and involve the provision of limiting nutrients (resources) to one species by another. It was recently shown in laboratory experiments that two species of pitcher‐dwelling crab spiders (Thomisidae), Thomisus nepenthiphilus and Misumenops nepenthicola, increased capture rates of flesh flies (Sarcophagidae) for their host, Nepenthes gracilis. The spiders ambushed pitcher‐visiting flesh flies, and dropped their carcasses into pitchers after consuming them. The consumption of shared prey resources by crab spiders and pitcher plants presents the possibility of parasitism between them. However, ecologically generalisable mechanisms that predict the context‐dependent outcomes of such mutualisms are not known. 2.The effectiveness framework (mutualism effectiveness = quality × quantity) is useful for examining the total effect of mutualisms, but its quality component can be difficult to define. We identify the crab spider–pitcher plant interaction as a type of resource conversion mutualism, and propose that the quality component in such interactions is the amount of the underlying resource contained in each unit of resource processed. We then used the crab spider–pitcher plant interaction to test the hypothesis that resource conversion mutualisms are more beneficial to the nutrient recipient when operating through high‐quality resources (i.e., large prey, in this interaction). 3.We sampled the prey and inquilines of 107 N. gracilis upper pitches in situ and analysed the differences between pitchers that were inhabited or uninhabited by crab spiders, and the differences between nutritional contents of prey that were consumed by crab spiders or not. 4.Pitchers inhabited by T. nepenthiphilus contained higher numbers of several prey taxa, many of which were flying insects. Consumption by T. nepenthiphilus reduced the nutrient contents in all prey examined. Overall, T. nepenthiphilus‐assisted prey capture is likely to result in a net nutrient gain for N. gracilis that is proportional to the size of prey consumed by T. nepenthiphilus 5.Our results suggest that resource conversion mutualisms are more likely to operate through high‐quality resources, since the nutrient‐processing species necessarily reduces the quality of the resource it processes while increasing its availability to the nutrient recipient species. This article is protected by copyright. All rights reserved.
... Larvae of X. beaveri construct sticky webs over the fluid surface of N. ampullaria (figure 1a) to ensnare emerging adult dipteran inquilines, mainly those of the Culicidae [4] and Phoridae (WN Lam 2017, personal observation). The niche of X. beaveri in pitcher-inquiline communities is comparable to that of other terrestrial, cross-habitat, inquiline predators such as the ant Camponotus schmitzi in Nepenthes bicalcarata [6], and crab spider Misumenops nepenthicola in Nepenthes gracilis [7]. These predators live outside of the aquatic pitcher phytotelma, but feed on its aquatic dipteran inhabitants. ...
Article
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The fluids of Nepenthes pitcher plants are habitats to many specialised animals known as inquilines, which facilitate the conversion of prey protein into pitcher-absorbable nitrogen forms such as ammonium. Xenoplatyura beaveri (Diptera: Mycetophilidae) is a predatory dipteran inquiline that inhabits the pitchers of N. ampullaria. Larvae of X. beaveri construct sticky webs over the fluid surface of N. ampullaria to ensnare emerging adult dipteran inquilines. However, the interaction between X. beaveri and its host has never been examined before, as it is not known if X. beaveri can contribute to nutrient sequestration in N. ampullaria. X. beaveri individuals were reared in artificial pitchers in the laboratory on a diet of emergent Tripteroides tenax mosquitoes, and the ammonium concentration of the pitcher fluids were measured over time. Fluid ammonium concentration in tubes containing X. beaveri were significantly greater than those of the controls. Furthermore, fluid ammonium concentrations increased greatly after X. beaveri larvae metamorphosed, although the cause for this increase could not be identified. Our results show that a terrestrial, inquiline predator can contribute significantly to nutrient sequestration in the phytotelma it inhabits, and suggest that this interaction has a net mutualistic outcome for both species.
... This is to certify that Ms. AnupriyaKarippadath of M.Sc. Biodiversity (2010-2012 has satisfactorily carried out the project entitled 'Ecology of Nepenthes khasiana inSouth Garo Hills : A study of habitat, associated organisms and trap morphology'as per the requirements of the University of Pune, as a part of her curriculum under our guidance ans supervision. ...
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Nepenthes khasiana is a carnivorous pitcher plant endemic to a part of the Indo-Burma hotspot in India. It is found in scattered populations across the state of Meghalaya. This is the first study focusing on macroecological aspects of this plant. The density of Nepenthes populations was found to be different in the 2 field sites chosen for field study. The soil characteristics, however, were similar in both sites, showing markedly poor phosphorous content. This was also true for the site with a cultivated N.khasiana population included in the study. Prey composition of the plant showed similarities to other pitcher plants, with Hymenoptera being the dominant taxon and 89% of prey being winged and capable of flight. 5 species of spiders were also found associated with N.khasiana. The liquid-filled pitchers of carnivorous plants form microecosystems with various interactions between plant, prey, inquilines and other associates. 3 species of dipteran larvae were ubiquitously found as metazoan inquilines in the pitchers of N.khasiana. Aspects of pitcher morphology and associated fauna were studied on the basis of hypotheses. The abundance of inquilines was found to be correlated negatively with the size of pitchers and it was also seen that the volume of digestive fluid is not correlated significantly with pitcher size. The strong positive correlation between size of open pitchers and duration of developmental period of pitchers suggests a tradeoff between size and rapidity of development, which is discussed in the context of other results obtained in this study.
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A new interaction between insects and carnivorous plants is reported from Brazil. Larvae of the predatory flower fly Toxomerus basalis (Diptera: Syrphidae: Syrphinae) have been found scavenging on the sticky leaves of several carnivorous sundew species (Drosera, Droseraceae) in Minas Gerais and São Paulo states, SE Brazil. This syrphid apparently spends its whole larval stage feeding on prey trapped by Drosera leaves. The nature of this plant-animal relationship is discussed, as well as the Drosera species involved, and locations where T. basalis was observed. 180 years after the discovery of this flower fly species, its biology now has been revealed. This is (1) the first record of kleptoparasitism in the Syrphidae, (2) a new larval feeding mode for this family, and (3) the first report of a dipteran that shows a kleptoparasitic relationship with a carnivorous plant with adhesive flypaper traps. The first descriptions of the third instar larva and puparium of T. basalis based on Scanning Electron Microscope analysis are provided.
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Phytotelmata habitats have been the focus of much research and are utilized by a wide variety of taxa. In the past 15 years numerous studies in many geographic regions and covering various types of phytotelmata have greatly increased our understanding of these unique habitats. The most recent summary of phytotelmata inhabitants included over 20 families of insects. A review of the literature and extensive work in lowland Ecuador shows the family level diversity is in fact at least twice that reported earlier. A reassessment of previous phytotelmata classification schemes, as well as an extensive bibliography, is provided.
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1. To improve our understanding of the relationship between the pitcher plant ( Sarracenia purpurea ) and the phytotelma community inhabiting its leaves we built an exploratory, mechanistic model based on stochiometric constraints on carbon and nitrogen associated with prey decomposition. 2. Our theoretical results suggest that the phytotelma community is acting as a mineralizing system producing nitrogen for the plant. This is confirmed by data collected in the field and in the literature, that show the amount of nitrogen produced by the decomposition of prey is sufficiently high to be considered as a major source of nitrogen for the plant. 3. In our model, nitrogen yield is higher if the phytotelma community is restricted to bacteria alone than when the full food web is present. Nitrogen availability is negatively affected by bacterivores (rotifers and protozoa mostly) and positively affected by a cascading effect of mosquito larvae. 4. When sedimentation rate is high, mosquitoes have a global positive effect on nitrogen production because they indirectly reduce the amount of nitrogen lost through sedimentation more than they export nitrogen through pupation. On the other hand, when sedimentation rate is low there is a hump-shaped relationship between the uptake rate of bacterivores by mosquito larvae and the nitrogen yield in the plant. 5. We conclude that plant–bacteria and plant–mosquito interactions are predominantly mutualistic, whereas plant–bacterivore interactions are predominantly parasitic. Our work also illustrates how ecosystem properties (here nitrogen production by the phytotelma community) can be understood as a function of trophic complexity and can be seen as a product of selection at the scale of a community.
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Observations of communities living in water held in the bracts of flowers of the wild banana, Heliconia bihai, in Puerto Rico show mosquito larvae to have very great influence in determination of community structure. These larvae quickly eliminate all or nearly all Protozoa and micro-Metazoa (other than arthropods) which, in the absence of mosquito larvae, are abundant in Heliconia-held water. Laboratory experiments support this conclusion.
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Understanding how communities respond to changes in temperature is a major challenge for community ecology. Temperature influences the relative degree to which top-down and bottom-up forces structure ecological communities. In greenhouse experiments using the aquatic community found in pitcher plants (Sarracenia purpurea), I tested how temperature affected the relative importance of top-down (mosquito predation) and bottom-up (ant carcasses) forces on protozoa and bacteria populations. While bottom-up effects did not vary consistently with temperature, the top-down effects of predators on protozoa increased at higher temperatures. These results suggest that temperature could change the relative importance of top-down and bottom-up effects in ecological communities. Specifically, higher temperature may increase the strength of top-down effects by raising predator metabolic rate and concomitant processes (e.g., activity, foraging, digestion, growth) relative to cooler temperatures. These findings apply broadly to an understanding of trophic interactions in a variable environment and are especially relevant in the context of ongoing climate change.
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The modern arachnids are the only group of arthropods in which the main organs of sight are camera-type eyes, not unlike our own, rather than compound eyes. The copepod crustaceans also lack compound eyes, but their nauplius eyes are rarely more than a trio of simple eye-cups, with a handful of receptors each. By contrast, spider eyes at their best have retinae with 103 to 104 receptors, and in the salticid Portia the inter-receptor angles may be as small as 2.4 min of arc (Williams and McIntyre 1980), which is only six times greater than in man (cone spacing 0.42 min), and is six times smaller than in the most acute insect eye (the dragonfly Aeschna, minimum inter-ommatidial angle 14.4 min; Sherk 1978). Thus, in some spiders, but by no means all, vision is excellent, and rivalled amongst invertebrates only by the cephalopod molluscs.
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Variation in 14 aquatic communities of dipterans in pitchers of 3 Nepenthes species was studied in Singapore. Communities in 3 clumps of Nepenthes ampullari Jack included 3 large aquatic predators, Toxorhynchites acaudatus (Leicester), Nepenthosyrphus sp., and Nepenthomyia sp. In communities in 2 clumps of Nepenthes rafflesiana Jack, another large aquatic predator, Pierretia sp., occurred at low rates; but the remaining 9 communities (3 N. ampullaria, 2 N. rafflesiana, and 4 N. gracilis Korth. clumps) lacked large aquatic predators. In 3 N. ampullaria communities with large aquatic predators, phorid density was low and 4-5 filter-feeder mosquito species coexisted. There, filter feeder communities were dominated by Tripteroides nepenthis (Edwards) and Uranotaenia moultoni Edwards; Tripteroides tenax (Meijere) and Culex eminentia (Leicester) together occupied <10%. In contrast, 11 other filter feeder communities were monopolized by T. tenax (3 communities), inhabited only by T. tenax and C. eminentia (3 communities), or T. tenax or C. eminentia (or both), occupied >8S% of 2-3 species (5 communities). Unique prey community structure in N. ampullaria clumps with large aquatic predators was attributed at least partly to selective removal of superior competitors by the predators and resultant colonization of inferior competitors more resistant to predation.
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The metazoan food webs of Nepenthes pitcher plants exhibit marked geographical variation In previous studies this was attributed lo a number of biogeographical factors including island area. local arthropod biodiversity and degrees of spatial and temporal variation of the host Nepenthes species. Recent investigations showed that some assumptions made in compiling these webs are erroneous and that predation is more widespread in these communities than previously assumed. In this study the new data are used to revise several webs from the geographical studies for comparison with the original versions. Conneetance values and predator:prey ratios increased significantly after revision (though all other food web statistics did not), providing evidence for widespread predation. This is presumed to be a result of some metazoan species adopting variable feeding strategies, depending on which food sources are available in their piteher. Despite this, the geographical patterns are still evident alter revision of the webs. Whether or not these are actually due to geographical Victors is discussed, h is suggested that the structure of Nepenthes webs is influenced by tour major factors- “geographical, deterministic, stochastic and host pitcher (the latter was discounted in previous studies), but that the relative importance of each factor is highly variable and cannot be quantified at present.
Article
. 1Two contrasting hypotheses concerning patterns in food web structure within pitchers of Nepenthes are tested using new information from six species of Nepenthes from Borneo.2In general, predictions that webs will be more complex, and the food chains they contain will be longer, the closer they are to the centre of Nepenthes species diversity, are supported.3For Nepenthes albomarginata, a widespread species with a distinctive north Bornean form, a contrasting pattern is evident explicable in terms of the morphology of the pitchers and local habitat preferences.4General explanations for food web patterns will always be susceptible to exception, reflecting nuances of natural history.