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

Published online by Cambridge University Press:  31 May 2011

Konstans Wells*
Biodiversity and Climate Research Centre (BiK-F), D-60325 Frankfurt (Main), Germany Sabah Parks, 88100 Kota Kinabalu, Sabah, Malaysia
Maklarin B. Lakim
Sabah Parks, 88100 Kota Kinabalu, Sabah, Malaysia
Stefan Schulz
Institute of Organic Chemistry, Technical University of Braunschweig, D-38106 Braunschweig, Germany
Manfred Ayasse
Institute of Experimental Ecology, University of Ulm, D-89081 Ulm, Germany
1Corresponding author. Email:


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.

Research Article
Copyright © Cambridge University Press 2011

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ACHARYA, K. K., ROY, A. & KRISHNA, A. 1998. Relative role of olfactory cues and certain non-olfactory factors in foraging of fruit-eating bats. Behavioural Processes 44:5964.CrossRefGoogle Scholar
BARTOLOMUCCI, A., DE, B. G. & FUCHS, E. 2001. How tree shrews (Tupaia belangeri) perform in a searching task: evidence for strategy use. Journal of Comparative Psychology 115:344350.CrossRefGoogle Scholar
BAUER, U., BOHN, H. F. & FEDERLE, W. 2008. Harmless nectar source or deadly trap: Nepenthes pitchers are activated by rain, condensation and nectar. Proceedings of the Royal Society B: Biological Sciences 275:259265.CrossRefGoogle ScholarPubMed
BENNETT, K. F. & ELLISON, A. M. 2009. Nectar, not colour, may lure insects to their death. Biology Letters 5:469472.CrossRefGoogle Scholar
BESTMANN, H. J., WINKLER, L. & VON HELVERSEN, O. 1997. Headspace analysis of volatile flower scent constituents of bat-pollinated plants. Phytochemistry 46:11691172.CrossRefGoogle ScholarPubMed
CHIN, L. J., MORAN, J. A. & CLARKE, C. 2010. Trap geometry in three giant montane pitcher plant species from Borneo is a function of tree shrew body size. New Phytologist 186:461470.CrossRefGoogle ScholarPubMed
CLARKE, C. 2006. Nepenthes of Borneo. Natural History Publications (Borneo), Kota Kinabalu. 207 pp.Google Scholar
CLARKE, C. M., BAUER, U., LEE, C. I. C., REMBOLD, K. & MORAN, J. A. 2009. Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters 5:632635.CrossRefGoogle Scholar
CORLETT, R. T. 2004. Flower visitors and pollination in the oriental (Indomalayan) region. Biological Reviews 79:497532.CrossRefGoogle ScholarPubMed
DI GIUSTO, B., GROSBOIS, V., FARGEAS, E., MARSHALL, D. J. & GAUME, L. 2008. Contribution of pitcher fragrance and fluid viscosity to high prey diversity in a Nepenthes carnivorous plant from Borneo. Journal of Biosciences 33:121136.CrossRefGoogle Scholar
DI GIUSTO, B., BESSIERE, J. M., GUEROULT, M., LIM, L. B. L., MARSHALL, D. J., HOSSAERT-MCKEY, M. & GAUME, L. 2010. Flower-scent mimicry masks a deadly trap in the carnivorous plant Nepenthes rafflesiana. Journal of Ecology 98:845856.CrossRefGoogle Scholar
DOMINY, N. J., SVENNING, J. C. & LI, W. H. 2003. Historical contingency in the evolution of primate color vision. Journal of Human Evolution 44:2545.CrossRefGoogle ScholarPubMed
EMMONS, L. H. 1991. Frugivory in tree shrews (Tupaia). American Naturalist 138:642649.CrossRefGoogle Scholar
EMMONS, L. H. 2000. Tupai: a field study of Bornean treeshrews. University of California Press, Berkeley, Los Angeles. 270 pp.Google Scholar
GOTELLI, N. J. & ELLISON, A. M. 2001. Evolutionary ecology of carnivorous plants. Trends in Ecology and Evolution 16:623629.Google Scholar
GRAFE, T. U., SCHÖNER, C. R., KERTH, G., JUNAIDI, A. & SCHÖNER, M. G. 2011. A novel resource–service mutualism between bats and pitcher plants. Biology Letters doi:10.1098/rsbl.2010.1141.CrossRefGoogle Scholar
HODGKISON, R., AYASSE, M., KALKO, E. K. V., HÄBERLEIN, C., SCHULZ, S., MUSTAPHA, W. A. W., ZUBAID, A. & KUNZ, T. H. 2007. Chemical ecology of fruit bat foraging behavior in relation to the fruit odors of two species of paleotropical bat-dispersed figs (Ficus hispida and Ficus scortechinii). Journal of Chemical Ecology 33:20972110.CrossRefGoogle Scholar
HUI, Y. H. 2010. Handbook of fruit and vegetable flavors. Wiley, Hoboken. 1095 pp.CrossRefGoogle Scholar
JOEL, D. M. 1988. Mimicry and mutualism in carnivorous pitcher plants (Sarraceniaceae, Nepenthaceae, Cephalotaceae, Bromeliaceae). Biological Journal of the Linnean Society 35:185197.CrossRefGoogle Scholar
JÜRGENS, A., EL-SAYED, A. M. & SUCKLING, D. M. 2009. Do carnivorous plants use volatiles for attracting prey insects? Functional Ecology 23:875887.CrossRefGoogle Scholar
KNUDSEN, J. T., ERIKSSON, R., GERSHENZON, J. & STÅHL, B. 2006. Diversity and distribution of floral scent. Botanical Review 72:1120.CrossRefGoogle Scholar
LIN, D. Y., ZHANG, S. Z., BLOCK, E. & KATZ, L. C. 2005. Encoding social signals in the mouse main olfactory bulb. Nature 434:470477.CrossRefGoogle ScholarPubMed
MERBACH, M. A., MERBACH, D. J., MASCHWITZ, U., BOOTH, W. E., FIALA, B. & ZIZKA, G. 2002. Mass march of termites into the deadly trap. Nature 415:3637.CrossRefGoogle ScholarPubMed
MORAN, J. A. 1996. Pitcher dimorphism, prey composition and the mechanisms of prey attraction in the pitcher plant Nepenthes rafflesiana in Borneo. Journal of Ecology 84:515525.CrossRefGoogle Scholar
NOR, S. M. 2001. Elevational diversity patterns of small mammals on Mount Kinabalu, Sabah, Malaysia. Global Ecology and Biogeography 10:4162.CrossRefGoogle Scholar
PALMER, T. M., STANTON, M. L. & YOUNG, T. P. 2003. Competition and coexistence: exploring mechanisms that restrict and maintain diversity within mutualist guilds. American Naturalist 162:S63S79.CrossRefGoogle ScholarPubMed
PHILLIPPS, A. & LAMB, A. 1987. Pitcher-plants of east Malaysia and Brunei. Nature Malaysiana 13:827.Google Scholar
RAGUSO, R. A. 2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annual Review of Ecology, Evolution, and Systematics 39:549569.CrossRefGoogle Scholar
RIEGER, J. F. & JAKOB, E. M. 1988. The use of olfaction in food location by frugivorous bats. Biotropica 20:161164.CrossRefGoogle Scholar
RÖCK, F., MUELLER, S., WEIMAR, U., RAMMENSEE, H. G. & OVERATH, P. 2006. Comparative analysis of volatile constituents from mice and their urine. Journal of Chemical Ecology 32:13331346.CrossRefGoogle ScholarPubMed
SCHAEFER, M. H. & RUXTON, G. D. 2008. Fatal attraction: carnivorous plants roll out the red carpet to lure insects. Biology Letters 4:153155.CrossRefGoogle ScholarPubMed
SCHAEFER, M. H., SCHAEFER, V. & VOROBYEV, M. 2007. Are fruit colors adapted to consumer vision and birds equally efficient in detecting colorful signals? American Naturalist 169:S159S169.CrossRefGoogle Scholar
STENSMYR, M. C., URRU, I., COLLU, I., CELANDER, M., HANSSON, B. S. & ANGIOY, A. M. 2002. Rotting smell of dead-horse arum florets – these blooms chemically fool flies into pollinating them. Nature 420:625626.CrossRefGoogle Scholar
STRAUSS, S. Y. & IRWIN, R. E. 2004. Ecological and evolutionary consequences of multispecies plant–animal interactions. Annual Review of Ecology, Evolution, and Systematics 35:435466.CrossRefGoogle Scholar
TIRINDELLI, R., DIBATTISTA, M., PIFFERI, S. & MENINI, A. 2009. From pheromones to behavior. Physiological Reviews 89:921956.CrossRefGoogle ScholarPubMed
VON HELVERSEN, O., WINKLER, L. & BESTMANN, H. J. 2000. Sulphur-containing “perfumes” attract flower-visiting bats. Journal of Comparative Physiology A – Sensory Neural and Behavioral Physiology 186:143153.CrossRefGoogle ScholarPubMed
VON STRALENDORFF, F. 1982. A behaviorally relevant component of the scent signals of male Tupaia belangeri – 2,5 dimethylpyrazine. Behavioral Ecology and Sociobiology 11:101107.CrossRefGoogle Scholar
WELLS, K., KALKO, E. K. V., LAKIM, M. B. & PFEIFFER, M. 2007. Effects of rain forest logging on species richness and assemblage composition of small mammals in Southeast Asia. Journal of Biogeography 34:10871099.CrossRefGoogle Scholar
WELLS, K., CORLETT, LAKIM, R. T.KALKO, M. B., E. K. V., & PFEIFFER, M. 2009. Seed consumption by small mammals from Borneo. Journal of Tropical Ecology 25:555558.CrossRefGoogle Scholar
WRIGHT, G. A. & SCHIESTL, F. P. 2009. The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Functional Ecology 23:841851.CrossRefGoogle Scholar