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Pitchers of Nepenthes rajah collect faecal droppings from both diurnal and nocturnal small mammals and emit fruity odour

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The pitchers of Nepenthes rajah, a montane carnivorous plant species from Borneo, are large enough to capture small vertebrates such as rats or lizards, which occasionally drown therein. The interactions of N. rajah with vertebrates, however, are poorly understood, and the potential mechanisms that lure vertebrates to the pitchers are largely unknown. We observed frequent visits (average: one visit per 4.2 h) of both the diurnal tree shrew Tupaia montana and the nocturnal rat Rattus baluensis to pitchers by infrared sensor camera and video recording. Both mammalian species often licked the inner surface of the pitcher lid, which harbours numerous exudate-producing glands. Analysis of volatiles extracted from the secretions of the pitcher lids by gas chromatography coupled to mass spectrometry (GC/MS) revealed 44 volatile compounds, including hydrocarbons, alcohols, esters, ketones and sulphur-containing compounds, which are commonly present in sweet fruit and flower odours. The faeces of small mammals were repeatedly observed inside the pitcher, whereas we found the body of only one Tupaia montana drowned in the 42, vital and reasonably large, surveyed pitchers. Our findings suggest that the N. rajah pitcher makes use of the perceptual biases of rats and tree shrews by emitting volatiles known from fruits. The profits that the plant obtains from the repeated visits of two small mammals, together with the provision of exudates for the mammals, comprise an exceptional case of plant–vertebrate interaction.
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Journal of Tropical Ecology (2011) 27:347–353. Copyright © Cambridge University Press 2011
doi:10.1017/S0266467411000162
Pitchers of Nepenthes rajah collect faecal droppings from both diurnal
and nocturnal small mammals and emit fruity odour
Konstans Wells,,1, Maklarin B. Lakim, Stefan Schulzand Manfred Ayasse§
Biodiversity and Climate Research Centre (BiK-F), D-60325 Frankfurt (Main), Germany
Sabah Parks, 88100 Kota Kinabalu, Sabah, Malaysia
Institute of Organic Chemistry, Technical University of Braunschweig, D-38106 Braunschweig, Germany
§Institute of Experimental Ecology, University of Ulm, D-89081 Ulm, Germany
(Accepted 11 March 2011)
Abstract: The pitchers of Nepenthes rajah, a montane carnivorous plant species from Borneo, are large enough to
capture small vertebrates such as rats or lizards, which occasionally drown therein. The interactions of N. rajah with
vertebrates, however, are poorly understood, and the potential mechanisms that lure vertebrates to the pitchers are
largely unknown. We observed frequent visits (average: one visit per 4.2 h) of both the diurnal tree shrew Tupaia
montana and the nocturnal rat Rattus baluensis to pitchers by infrared sensor camera and video recording. Both
mammalian species often licked the inner surface of the pitcher lid, which harbours numerous exudate-producing
glands. Analysis of volatiles extracted from the secretions of the pitcher lids by gas chromatography coupled to mass
spectrometry (GC/MS) revealed 44 volatile compounds, including hydrocarbons, alcohols, esters, ketones and sulphur-
containing compounds, which are commonly present in sweet fruit and flower odours. The faeces of small mammals
were repeatedly observed inside the pitcher, whereas we found the body of only one Tupaia montana drowned in the
42, vital and reasonably large, surveyed pitchers. Our findings suggest that the N. rajah pitcher makes use of the
perceptual biases of rats and tree shrews by emitting volatiles known from fruits. The profits that the plant obtains
from the repeated visits of two small mammals, together with the provision of exudates for the mammals, comprise an
exceptional case of plant–vertebrate interaction.
Key Words: carnivorous plants, extrafloral nectaries, plant–animal interaction, Rattus baluensis,Tupaia montana
INTRODUCTION
Pitchers of Nepenthes plants are intricate traps that have
evolved various mechanisms to lure their animal prey into
the pitcher as a valuable nutritional resource in habitats
withnutrient-deficientsoils(Clarke2006,Gotelli&Ellison
2001). The jug-shaped pitcher organ, which grows as a
distal extension of a leaf, usually contains digestive fluids
ready to process material from animals drowned inside
the pitcher. Notably, Nepenthes species produce extrafloral
nectariesthat lie beneath the lid or the fringe of the pitcher,
the so-called peristome (Bauer et al. 2008, Di Giusto et al.
2008, Moran 1996) and that provide arthropods and
small mammals with a rewarding resource (Clarke et al.
2009, Joel 1988).
1Corresponding author. Email: konstans.wells@senckenberg.de
The first step, however, is to attract suitable prey
to the pitcher. Most of the carnivorous plant species
studied to date promote their detection by ants and other
arthropods through olfactory and visual cues (Bauer et al.
2008, Bennett & Ellison 2009, Di Giusto et al. 2008,
2010; Joel 1988, J ¨
urgens et al. 2009, Merbach et al.
2002, Moran 1996, Schaefer & Ruxton 2008). Whereas
such mechanisms of prey attraction and capture through
visual and olfactory cues and occasional rewards have
long been examined in arthropod-capturing plants, only
recent studies have explored previously anecdotal records
of small-mammal interactions with pitcher plants. The
montanetreeshrew,Tupaia montana, has frequently been
found to approach pitchers of the three large montane
species Nepenthes lowii,N. rajah and N. macrophylla from
Borneo and defecate into the pitcher while licking its lid
(Chin et al. 2010, Clarke et al. 2009) and the bat Kerivoula
hardwickii roosts and defecates into aerial pitcher of N.
rafflesiana var. elongata (Grafe et al. 2011). Nepenthes rajah
348 KONSTANS WELLS ET AL.
is one of the most spectacular species because of its large
pitchers, which can hold up to 2 L of fluid, and because
of the occasional observations of drowned vertebrates
therein (Clarke 2006, Phillipps & Lamb 1987). Since fea-
tures such as intense pitcher colouration and extrafloral
nectaries have evolved in congeneric species for arthropod
attraction but are not reduced in N. rajah and other large
species, some functionality in either attracting arthropods
or even vertebrates can be hypothesized.
In this study, we investigated the interactions of N.
rajah with small mammals and explored whether pitchers
were visited by small-mammal species others than T.
montana. For diurnal mammals and birds with well-
developed colour vision, colour has been identified as
the major signal to the consumer in plant advertisement
(Dominy et al. 2003, Schaefer et al. 2007). However,
pitchers are often hidden within dense grassy vegetation.
Moreover, if pitchers are visited by both diurnal and
nocturnal mammals for which olfaction is a major sensory
modality (Acharya et al. 1998, Hodgkison et al. 2007,
Rieger & Jakob 1988), olfactory cues may serve as
a general mechanism for attracting both diurnal and
nocturnal visitors. Emission of fruit and flower scent by
the closely related arthropod-capturing N. rafflesiana,as
recently reported by Di Giusto et al. (2010), leads to the
question if such kind of odours are also emitted from
N. rajah. Tree shrews, squirrels and rats are likely to
share some resources such as various fruits as known
from nearby rain-forest localities (Emmons 2000, Nor
2001, Wells et al. 2009). Therefore, we have analysed
volatile compounds emitted from the pitcher lid of plants
frequently visited by small mammals as a first step
to exploring potential general signals attracting small
mammals to the pitcher.
METHODS
Study site, field observations and sample collection
Field work was conducted at Mesilau (060252N,
1163557E, c. 2000 m asl) near Mount Kinabalu
in Sabah, Borneo, between 2 December 2009 and 24
January 2010. The study area comprised a natural
landslip of loose ultrabasic soil on a slope surrounded
by pristine montane forest within the Kinabalu National
Park area. Although Nepenthes rajah occurs naturally
in such habitat and is endemic to the Kinabalu Park
area, some of the population in our study area have
been planted along a trail to make this spectacular
species accessible to tourists. For all field experiments,
we therefore selected pitchers away from the trail in
order to avoid disturbance by tourists. We recorded visits
of small mammals to four lower pitchers of different
plant individuals of mature Nepenthes rajah plants. The
glands beneath the lids of these pitchers produced a
visible liquid film and were assumed to provide exudates
to potential visitors. Digital camera traps with infrared
sensors (Cuddeback Capture IR 3.0, USA) were set to a
picture interval of 30 s. We considered all pictures taken
5 min after the previous one as a new visit. Recordings
were made for 77 to 96 observational hours per pitcher
(mean =87 ±10), resulting in a total recording time of
348 h. We further recorded small-mammal visits to four
other pitchers with a video camera (Sony, DCR-SR-45E,
Japan) with an additional recording time of 55 h. We
conducted equal amounts of recording during daytime
and night-time. For results, means are given with 1
SD. We recorded the frequency of faecal droppings in
pitchers by a daily survey of seven pitchers of different
plant individuals in which we placed a plastic sheet above
the fluid in order to collect fresh droppings for a total
of 61 observation days. Species identification of small
mammals from digital records and the assignment of
faecal droppings to its originator were facilitated by live
trapping in the nearby forest environment as part of our
small-mammal monitoring efforts (Wells et al. 2007).
We extracted the compounds of lids in pentane or
acetone for later gas chromatography (GC) and GC/mass
spectrometry in the laboratory. For this, lids were cut
off during the day and wrapped in aluminium foil to
avoid contamination. On returning to the field laboratory
30–60 min later, lids were extracted in vials containing
20–30 ml of pentane (R & M Marketing, Essex, UK,
99%) or acetone (Fisher Scientific, UK, 99.8+%) for c.
30 min. Extracts were stored in airtight glass vials closed
with Teflon-coated lids. For chemical analysis, we used
one acetone and one pentane sample, which revealed
similar results and we therefore present the overall list
of compounds without further differentiation.
Gas chromatography/mass spectrometry
Analyses of the lid extracts was performed with a HP 6890
gas chromatograph (Hewlett Packard, Series, Palo Alto,
CA, USA) connected to a mass selective detector (GC/MS,
Agilent Quadrupol 5972) equipped with a polar DB-Wax
column (J & W Folsom, USA) with an inner diameter
of 0.25 mm, a length of 30 m, and a film thickness of
0.25 μm. The flow rate of the carrier gas (nitrogen) was
1.5 ml min1constant flow. One microlitre of each sample
was injected in full at 50 C. After 1 min, the splitter
was opened, and the oven temperature increased at a
rate of 10 Cmin
1to 240 C. Structure elucidation of
individual compounds was carried out by a comparison of
mass spectra and retention times of natural products with
corresponding data of synthetic reference samples, with
the NIST database, and with a database of the Institute of
Experimental Ecology.
Small-mammal interactions with Nepenthes rajah 349
Figure 1. Interactions of Tupaia montana with Nepenthes rajah. Individuals of T. montana usually sit on the pitcher rim while licking the lid of a pitcher
(a). We found one individual of T. montana drowned inside a pitcher of N. rajah (b). Faecal droppings from small mammals can be seen at the bottom
of the lid, fresh droppings were also observed 14 d after the tree shrew was found drowned. Scale bars (bottom left) represent c.1cm.
RESULTS
Pitcher visits by rats and tree shrews
Field observations revealed that small mammals
frequently visited pitchers of Nepenthes rajah. We recorded
a total of 56 visits of the tree shrew Tupaia montana
and 42 visits of the rat Rattus baluensis within 413.5 h
of observation (average of one visit per 4.2 h). In
most interactions, individuals of both T. montana and
R. baluensis positioned themselves with all four feet on
the peristome of the pitchers in order to lick parts of
the inner surface of the pitcher lid (Figures 1 and 2).
Several individuals of both species appeared to be involved
in the interactions; although we were not able to fully
distinguish individuals, encountered rats differed in the
size of testes and tree shrews in body size. From this
position, faecal pellets produced by the tree shrew or
rat could easily fall directly down into the pitcher.
Occasionally, the animal moved its front feet further
upward to lick the upper part of lids that were up to
210 mm long. Interactions lasted for only 2–39 s for the
tree shrew (mean =19 ±12 s, n =18 video recordings)
and 11–20 s in the rat (mean =18 ±7s,n=17).
Tree shrews visited pitchers throughout the day
between 06h00 and 17h45 with an average observed
time interval of 133 ±111 min (n =37) between
consecutive visits of the same pitcher. Similarly, rats
visited pitchers throughout the night and late afternoon
between 17h00 and 05h30 with an average observed
time interval of 166 ±99 min (n =29) between
consecutive visits.
We observed fresh faecal droppings from both tree
shrews and rats inside the surveyed pitchers with an
overall frequency of new faecal droppings every 3.4 d.
The pitcher that received most faecal droppings contained
new droppings on seven out of nine observation days,
suggesting that attractive pitchers can expect a relatively
continuous intake of faeces.
We found only one drowned Tupaia montana inside
a large pitcher (inner diameter of pitcher rim: 110 ×
85 mm, Figure 1b) in the 42 mature pitchers that we
surveyed repeatedly during field work. Various dipteran
flies and midges were frequently observed in pitchers
containing faeces and the decaying tree shrew, whereas
they appeared to be absent from pitchers with clear liquid
and no animal content. Fresh faecal droppings on the
bottom of the lid with the drowned animal were observed
14 d after observing the drowned tree shrew, suggesting
that this pitcher was still attractive to small mammals.
Analysis of volatile compounds
In the samples from pitcher lids of plants frequently visited
by small mammals, we detected a total of 44 volatile
350 KONSTANS WELLS ET AL.
Figure 2. Rattus baluensis licking the lid of a Nepenthes rajah pitcher while sitting on the pitcher rim. Note the faecal pellet at the anus of the rat; this
pellet is ready to drop inside the pitcher during the feeding event. The scale bar (bottom left) represents c.1cm.
compounds (Appendix 1). Hydrocarbons, alcohols, esters
and ketones were among the most commonly found
compounds in terms of numbers and the relative amount
in samples. Further, we identified six sulphur-containing
compounds. The odour of N. rajah which is perceptible by
human nose is only slight fruity and but appears to have
a component resembling the odour of cabbage from the
genus Brassica.
DISCUSSION
Interactions of carnivorous plants with vertebrates are
rare and remain little investigated. An important factor
in understanding the strength and mechanism of such
interactions is the number of species involved, since
multispecies interactions largely influence the strength
and coevolution of pairwise interactions (Palmer et al.
2003, Strauss & Irwin 2004) and, hence, the way that
carnivorous strategies of the attraction and capture of
resources evolve. Our study shows that not only the tree
shrew Tupaia montana, but also the rat Rattus baluensis,
frequently interacts with pitchers of Nepenthes rajah.Small
mammals appear to be attracted to the pitchers, and,
while licking-off exudates produced by the pitcher lid,
they repeatedly drop faeces inside the pitcher. The major
interaction between N. rajah and small mammals appears
therefore to be a resource exchange on a mutualistic
basis – extrafloral nectar for faecal droppings. This
mutualistic interaction and the function of the pitcher
as a collecting tank for faecal droppings is in accordance
with studies by Chin et al. (2010) and Clarke et al.
(2009), except that we found N. rajah also to be visited
by nocturnal rats and not to be specialized to tree shrews
as suggested by these studies. Moreover, the occasional
capture of visiting small mammals together with the
relatively large opening of the pitcher suggest that N. rajah
is not as a whole specialized for coprophagy. Indeed, this
large pitcher with a relatively unspecified wide opening
not only seems to be advantageous for collecting faeces
from various small-mammal species that differ in size
and behaviour, but also might favour a cascade of effects
in collecting and processing additional animal material,
once faecal droppings influence the milieu inside the
pitcher liquid; pitchers that contained collected faeces or
the drowned tree shrew appeared to be more frequently
visited by various species of dipteran flies and midges,
some of which were also found to have drowned in the
liquid (pers. obs.).
Although cost–benefit models in carnivorous plant
interactions generally remain poorly understood (Gotelli
& Ellison 2001), the exploration of systems in which
vertebrates are involved awaits substantial future
research, since even basic knowledge of the ecology and
life history of small tropical mammals is sparse. Whereas
rat and tree shrew species in tropical rain forests are
known to overlap in their use of resources and habitats
(Emmons 2000, Nor 2001, Wells et al. 2009), tree shrews,
for example, have weaker teeth and relatively simple
intestines with short retention times (Emmons 1991); this
Small-mammal interactions with Nepenthes rajah 351
might impact the interaction with N. rajah with respect
to the likelihood of defecating or the amount of faeces
dropped into the pitcher during a visit to the plant. In turn,
the various needs and limits of small-mammal species
in the montane environment might affect the relative
attraction of visits to the pitcher plants in relation to
foraging time allocated to alternative resources. Small
mammals are probably not only attracted, but also gain
rewardsbyconsumingextrafloralnectarsfromthepitcher
lid. Given the relatively large number of daily visits to
pitchers compared with the few animal ranges likely to
occur in the study area of approximately 1 ha (Emmons
2000), only a limited number of animals probably are
repeatedly visiting the pitchers, an undertaking that they
should perform only if previous visits have been beneficial
to them (Wright & Schiestl 2009). Certainly, N. rajah
needs to be efficient at attracting small mammals that can
be expected to feed on variable animal and plant resources
in the surrounding environment. Frequent pitcher visits
are thus unlikely to occur by chance or if the pitchers are
difficult to detect by animals. Small mammals might be
attracted by both the visual and olfactory cues of pitcher
plants. Our odour analysis has revealed that a diverse
odour of not less than 44 different compounds is emitted
by the lids of N. rajah. Initial behavioural tests in the
field revealed only weak evidence that small mammals
are solely attracted by scent (i.e. bioassay with covered
and dislocated lids versus controls), but more research is
needed to disentangle the strength of olfactory and visual
cues and the possible role of particular compounds. In
particular, a more detailed sampling procedure including
so-called headspace samples may reveal a larger spectra of
volatile odours not captured with our sampling protocol
and additional compounds may be emitted from the
peristome such as in N. rafflesiana (Di Giusto et al. 2010).
Someofthecompounds,suchasnonanal, 2-methylpropyl
acetate, benzyl alcohol, or acetophenone emitted by N.
rajah, occur in various fruit and flowers of unrelated
plant species (Hui 2010, Knudsen et al. 2006). These
results are in accordance with the recent finding that
N. rafflesiana emits flower and fruit odour in order to
attract various arthropod species (Di Giusto et al. 2010).
The overlap in volatile compounds of the two Nepenthes
species, viz. N. rajah and N. rafflesiana investigated to
date, included nonanal and acetophenone beside the
ubiquitous compounds hexadecane and benzyl alcohol.
Notably, we have identified six sulphur-containing
compounds in the bouquet of N. rajah, whereas no such
compounds have been detected in N. rafflesiana (Di Giusto
et al. 2010). Sulphur-containing compounds have also
been found to be associated with the attraction of flower-
visiting bats (Bestmann et al. 1997, von Helversen et al.
2000). Dimethyl disulphide present in mouse urine might
also play a role in mammalian social behaviour (Lin et al.
2005) and attracts flies to flowers of the dead-horse arum
Helicodiceros muscivorus (Stensmyr et al. 2002). To the
best of our knowledge, however, none of the sulphur-
containing compounds that we have determined in our
study has been reported, to date, as a key substance in
social behaviour or as flower content (Knudsen et al.
2006). Only 3-hydroxy-2-butanone found in the scent
of Tupaia belangeri (von Stralendorff 1982) and 2-
furanmethanol found in laboratory mouse scent (R¨
ock
et al. 2006) are among the volatiles in our sample,
also recorded from mammals. However, both volatiles
are also present in flowers (Knudsen et al. 2006). As
shown for dimethyl disulphide, which occurs in both
rotten flesh and flowers and attracts glossophagine bats,
the effects of substances in odours are largely context-
dependent. Another interesting aspect for future research
is the occurrence of fatty acid derivatives such as the
isobutyl esters, which might eventually have a role as
a lipid complement in the diet of small-mammal visitors.
The role of scent signals of flowers and fruits remains
surprisingly poorly investigated for terrestrial small
mammals compared with those for bats or arthropods
(Corlett 2004, Raguso 2008) despite the well-developed
olfactory senses in small mammals (Tirindelli et al. 2009).
The rich odour of N. rajah lids with many volatiles that are
also found in flowers and fruits and that attract animal
partners is however a first preliminary indication that
olfactory cues may play a role in attracting both tree
shrews and rats to the pitcher.
In summary, the pitcher plant Nepenthes rajah is
frequently visited by diurnal tree shrews and nocturnal
rats that drop faeces into the pitcher while licking the
lid that produces extrafloral nectaries. Although our
results add to the little information available concerning
the interaction of vertebrates with carnivorous plants,
much more research is needed to establish the response
of small-mammal species to particular volatiles and to
determine whether species from different taxa respond to
the same visual and olfactory cues. Laboratory studies
suggest that nocturnal mice rely much more on olfactory
cues than diurnal tree shrews, which in turn rely more
on visual cues (Bartolomucci et al. 2001). Plasticity in
volatile emission during the day and night or among
various stages of life would be of great interest given
the various life histories of the small-mammal species
involved. Moreover, on the basis that a faecal drop into
the pitcher not only adds to the bouquet surrounding
the pitcher, but also provides a saprobic milieu for other
species to join, species interactions and trophic cascades
at pitchers need to be explored from various perspectives.
ACKNOWLEDGEMENTS
We are delighted to thank the staff of Sabah Parks,
particularly Fred Tuh Yit Yuh, Alim Biun, and Ansou
352 KONSTANS WELLS ET AL.
Gunsalam, for their varied support during field work
and for their amicable hospitality. K. Eduard Linsenmair,
Brigitte Fiala, Jorimia Molubi, and Martin Pfeiffer are
acknowledged for logistic support during field work. We
thank Andrea Weis for assisting with laboratory analysis.
We thank the anonymous reviewers for providing helpful
comments on an earlier draft of the manuscript.
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Appendix 1.
Volatile compounds emitted from the pitcher lids of Nepenthes rajah
frequently visited by tree shrews and rats. The following compounds
were found (retention times for a: acetone and p: pentane are given in
parentheses; note that there were unknown positions of double bonds
for the three esters at retention times of 2529, 2643, 2713). Out of
these compounds, at least 16 have been recorded in fruits or flowers
according to Knudsen et al. (2006) and the pherobase (database of insect
pheromones and semiochemicals, http://www.pherobase.com) and at
least 14 are also recorded as semiochemicals in arthropod interactions
according to the pherobase.
Hydrocarbons: hexadecane (1597, p), heptadecane (1698, p),
octadecane (1798, p), pentacosane (2500, p), heptacosane (2700, a, p),
octacosane (2800, p), nonacosane (2900, a,p), triacontane (3000, p),
hentriacontane (3090, p).
Diols and their derivatives: 3-hydroxy-2-butanone (1297, a), 4-
hydroxy-2-pentanone (1466, a), 2,3-butanediol (1542, a), 2,3-dihydro-
3,5-dihydroxy-6-methyl-4H-pyran-4-one (2274, a).
Esters: isobutyl acetate (1024, a), isobutyl decanoate (1755, p),
ethyl dodecanoate (1844, p), bis-isobutyl butanedioate (1906, p),
isobutyl dodecanoate (1960, p), 3-methylbutyl dodecanoate (2068,
p), 2-butyl butanedioate (2009, p), ethyl tetradecanoate (2048, p),
bis-isobutyl hexanedioate (2130, p), isobutyl tetradecanoate (21.645,
p), 3-methylbutyl tetradecanoate (22.726, p), isobutyl hexadecanoate
(23.683, p), 2-butyl tetradecanoate (2166, a), ethyl hexadecanoate
(2254, p), ethyl octadecanoate (2481, a,p), ethyl octadecadienoate
(2529, p), isobutyl octadecanoate (2594, p), isobutyl octadecadienoate
(2643, p), isobutyl octadecatrienoate (2713, p), octadecenoic acid ester
(2974, p).
Acids: acetic acid (1468, p).
Aldehydes: nonanal (1395, p), octacosanal (3396, p), triacontanal
(>3600, p).
Aromatic compounds: acetophenone (1655, p), N-ethyl-benzamine
(1730, p), benzyl alcohol (1879, p).
Sulphur-containing compounds: diethyl disulphide (1214, p), ethyl
1-methyl ethyl disulphide (1259, p), bis-1-methylethyl sulphide (1261,
p), diethyl trisulphide (1514, p), ethyl 1-methylethyl trisulphide (1527,
p), bis-1-methylethyl trisulphide (1535, p); others: furan (1611, p), 2-
furanmethanol (1661, a).
... Recently, it could be demonstrated that not only arthropods but also small mammals are attracted by the nectar-producing pitchers of some Bornean Nepenthes species (Clarke et al., 2009). In turn, the visiting mammals leave fecal droppings in the pitchers that serve as essential nitrogen source for the carnivorous pitcher plants (Greenwood et al., 2011;Wells et al., 2011). ...
... While various arthropods, such as ants and flies, are meant to fall in the pitchers, also small visiting vertebrates may accidentally fall in the fluid-filled pitchers and eventually serve as "prey" if they should not be able to escape the trap. Such rare cases have repeatedly been reported for rats (e.g., Rattus baluensis; see Spenser, 1862;Phillipps, 1988), mountain tree shrews (Tupaia montana; Wells et al., 2011) and even a bird has been found in a pitcher plant (Hewitt-Cooper, 2012), though the latter incidence occurred in cultivation and not in the wild. Recently, also the first gecko was found drowned in a pitcher of N. mirabilis in Guangdong Province, southern China (Hua et al., 2013). ...
... Usually, if vertebrates are found in Nepenthes, they are trapped in very large pitchers, such as in the Bornean N. rajah and N. rafflesiana (e.g., Wells et al., 2011). The pitchers of N. treubiana, however, are merely of average size reaching about 20 cm in height. ...
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We report on the second known case of a drowned gecko specimen being accidentally trapped in a pitcher plant. In August 2013, a dead specimen of Lepidodactylus cf. lugubris was found in a pitcher of Nepenthes treubiana near Kokas on the Onin (Fakfak) Peninsula of the Indonesian part of New Guinea.
... Several montane species (N. lowii, N. macrophylla and N. rajah) acquire a significant proportion of nitrogen from the capture of faeces of mammals such as Tupaia montana or Rattus baluensis (Clarke et al. 2009;Chin, Moran & Clarke 2010;Wells et al. 2011). ...
... It is notable that all known coprophagous Nepenthes species, including N. hemsleyana, that have outsourced prey capture to mammals, exploit their partners' sensory system to attract them (Wells et al. 2011;Moran et al. 2014;Sch€ oner et al. 2015c;Sch€ oner, Simon & Sch€ oner 2016). In exchange, these pitcher plants receive multiple benefits: all associated mammals have foraging areas that most likely exceed the catchment area of the plants' arthropod attractants by far. ...
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1. Mutualisms are interspecific interactions where each of the species involved gains net benefits from the other(s). The exchange of resources and/or services between mutualistic partners often involves tasks that species originally accomplished themselves but which have been taken over by or transferred to the more efficient partner during the evolution of the mutualism. Such ‘ecological outsourcing’ can be seen, for example, in several carnivorous plants that have transferred prey capture and digestion to animal partners. However, the outcome of this transfer and its fitness relevance has rarely been quantified. 2. Using a digestive mutualism between a carnivorous pitcher plant (Nepenthes hemsleyana) and a bat (Kerivoula hardwickii) as a model, we tested the hypothesis that ecological outsourcing is a profitable strategy for the outsourcing partner. To evaluate the value of this mutualism, we conducted a series of field and glasshouse experiments. We measured the benefits of ecological outsourcing by comparing survival, growth, photosynthesis and nutrient content of N. hemsleyana plants fed with bat faeces to those fed with arthropods. To investigate the costs of such outsourcing processes, we repeated the experiment with the closest relative (Nepenthes rafflesiana) that is not adapted to digest bat faeces. 3. We found that N. hemsleyana plants fed with faeces had increased survival, growth and photosynthesis compared to plants fed with arthropods only. On average, plants covered 95% of their nitrogen demand from faeces under strong nutrient deprivation. Despite N. rafflesiana's higher arthropod capture rate, faeces covered a large part of this species’ nutrient demand as well, suggesting low costs for outsourcing. 4. Synthesis. Outsourcing prey capture and digestion to the mutualism partner seems to be a beneficial strategy for N. hemsleyana. It may explain the evolutionary trend of several carnivorous plants to lose their carnivorous traits while increasing their attractiveness to mutualistic partners. On a much broader scale, we propose that ecological outsourcing could be one of the major drivers for the evolution and maintenance of mutualisms.
... Tambuyukon, we recorded it as low as 2,040 m (Table 1) and the lowest records from Mt. Kinabalu are around 2,100 (Musser, 1986;Phillipps & Phillipps, 2016), although it has been observed with camera traps just over 2,000 m in association with pitcher plants (Greenwood, Clarke, Ch'ien, Gunsalam, & Clarke, 2011;Wells, Lakim, & Beaucournu, 2011;Wells, Lakim, Schulz, & Ayasse, 2011). At these lower elevations, it is scarce, but becomes much more abundant in upper montane dwarf forest and scrubland, up to the summit on Mt. ...
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... In the case of highland Nepenthes that have resourceexchange mutualistic associations with small terrestrial mammals (N. lowii, N. rajah, and N. macrophylla), pitcher shape, proportions, scent and color are finely tuned to the geometry and sensory modalities of their mammalian partners [77][78][79]83]. It is unlikely that hybrids between these and more "typical" species would produce pitchers of the required geometry to maintain this association. ...
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... Cheek (2015) Malaysia Copper accumulation in ultramafic plants van der Ent and Reeves (2015) Discovery of nickel hyperaccumulators Hoffmann et al. (2003), van der Ent and Mulligan (2015), van der Ent et al. ( , 2016b Ecology of nickel hyperaccumulators: nickel insects van der Ent et al. (2015f ) Floristics, plant-soil relations, ultramafic endemism Chen et al. (2014), Fowlie (1985), Peng et al. (2015), Proctor et al. (1988aProctor et al. ( , b, 1989 Ultramafic forest vegetation structure, plant ecology, community ecology Adam (2002), Aiba et al. (2015), Aiba and Kitayama (1999), Brearley (2005), Bruijnzeel et al. (1993), Kitayama (1992), Proctor et al. (1988a, b), Sawada et al. (2015), Tashakor et al. (2013), van der Ent et al. (2015avan der Ent et al. ( , b, f, 2016a Ultramafic geochemistry Tashakor et al. (2011Tashakor et al. ( , 2013 Ultramafic plant-other biota interactions Wells et al. (2011) Ultramafic-associated insects and soil invertebrates Chung et al. (2013), Hasegawa et al. (2006), Jones et al. (2010), Leakey and Proctor (1987) Myanmar Mineralogy of jadeitite and related rocks, including serpentinites Shi et al. (2012) Pakistan Ultramafic geochemistry and soil-plant metal relations Kfayatullah et al. (2001), Naseem et al. (2009), Shah et al. (2010 Information within columns organized in alphabetical order Table 1 continued ...
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