Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T14:23:20.577Z Has data issue: false hasContentIssue false
  • English
  • Français

The plant-ant Camponotus schmitzi helps its carnivorous host-plant Nepenthes bicalcarata to catch its prey

Published online by Cambridge University Press:  17 December 2010

Vincent Bonhomme ,
Isabelle Gounand ,
Christine Alaux ,
Emmanuelle Jousselin ,
Daniel Barthélémy  and
Laurence Gaume
Vincent Bonhomme*
Affiliation:
Université Montpellier II, CNRS, INRA, UMR AMAP: Botanique et Bioinformatique de l'Architecture des Plantes, CIRAD – TA A51/PS2 Boulevard de la Lironde, F-34398 Montpellier Cedex 5, France
Isabelle Gounand
Affiliation:
Université Montpellier II, CNRS, INRA, UMR AMAP: Botanique et Bioinformatique de l'Architecture des Plantes, CIRAD – TA A51/PS2 Boulevard de la Lironde, F-34398 Montpellier Cedex 5, France
Christine Alaux
Affiliation:
Université Montpellier II, CNRS, INRA, UMR AMAP: Botanique et Bioinformatique de l'Architecture des Plantes, CIRAD – TA A51/PS2 Boulevard de la Lironde, F-34398 Montpellier Cedex 5, France
Emmanuelle Jousselin
Affiliation:
INRA, UMR CBGP, Campus International de Baillarguet, CS 30016, 34988 Montferrier-sur-Lez, France
Daniel Barthélémy
Affiliation:
Université Montpellier II, CNRS, INRA, UMR AMAP: Botanique et Bioinformatique de l'Architecture des Plantes, CIRAD – TA A51/PS2 Boulevard de la Lironde, F-34398 Montpellier Cedex 5, France
Laurence Gaume
Affiliation:
Université Montpellier II, CNRS, INRA, UMR AMAP: Botanique et Bioinformatique de l'Architecture des Plantes, CIRAD – TA A51/PS2 Boulevard de la Lironde, F-34398 Montpellier Cedex 5, France
*
*Corresponding author. Email: Vincent.Bonhomme@cirad.fr
Get access Rights & Permissions [Opens in a new window]

Abstract:

The Bornean climber, Nepenthes bicalcarata, is unique among plants because it is both carnivorous and myrmecophytic, bearing pitcher-shaped leaves and the ant Camponotus schmitzi within tendrils. We explored, in the peat swamp forests of Brunei, the hypothesis that these ants contribute to plant nutrition by catching and digesting its prey. We first tested whether ants increased plant's capture rate. We found that unlike most plant-ants, C. schmitzi do not exhibit dissuasive leaf-patrolling behaviour (zero patrol on 67 pitchers of 10 plants) but lie concealed under pitcher rim (13 ± 6 ants per pitcher) allowing numerous insect visits. However, 47 out of 50 individuals of the largest visitor dropped into the pitchers of five plants were attacked by ants and the capture rate of the same pitchers deprived of their ambush hunting ants decreased three-fold. We then tested whether ants participated in plant's digestion. We showed in a 15-d long experiment that ants fed on prey and returned it in pieces in seven out of eight pitchers. The 40 prey deposited in ant-deprived pitchers remained intact indicating a weak digestive power of the fluid confirmed to be only weakly acidic (pH ~5, n = 67). The analysis of 10 pitcher contents revealed that prey, mainly ants and termites, was very numerous (~400 per pitcher per plant) and highly fragmented. Altogether, these data suggest a positive effect of C. schmitzi on both prey intake and breakdown. This ant–plant interaction could thus be a nutritional mutualism involving the unusual association of carnivory and myrmecotrophy.

Keywords

Ant-plant mutualismmyrmecophytemyrmecotrophypitcher plantpredation strategy
Type
Research Article
Information
Journal of Tropical Ecology , Volume 27 , Issue 1 , January 2011 , pp. 15 - 24
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

AN, C.-I., FUKUSAKI, E.-I. & KOBAYASHI, A. 2002. Aspartic proteinases are expressed in pitchers of the carnivorous plant Nepenthes alata Blanco. Planta 214:661–667.CrossRefGoogle ScholarPubMed
ATHAUDA, S. B. P., MATSUMOTO, K., RAJAPAKSHE, S., KURIBAYASHI, M., KOJIMA, M., KUBOMURA-YOSHIDA, N., IWAMATSUI, A., SHIBATA, C., INOUE, H. & TAKAHASHI, K. 2004. Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases. Biochemical Journal 381:295–306.CrossRefGoogle ScholarPubMed
BAUER, U., WILLMES, C. & FEDERLE, W. 2009. Effect of pitcher age on trapping efficiency and natural prey capture in carnivorous Nepenthes rafflesiana plants. Annals of Botany 103:1219–1226.CrossRefGoogle ScholarPubMed
BEATTIE, A. 1989. Myrmecotrophy: plants fed by ants. Trends in Ecology and Evolution 4:172–176.CrossRefGoogle ScholarPubMed
BEAVER, R. A. 1983. The communities living in Nepenthes pitcher plants: fauna and food webs. Pp. 129–160 in Frank, J. H. & Lounibos, L. P. (eds.). Phytotelmata: terrestrial plants as hosts for aquatic insect communities. Plexus Publishing, Inc., Medford. 293 pp.Google Scholar
BOHN, H. F. & FEDERLE, W. 2004. Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Proceedings of the National Academy of Sciences USA 101:14138–14143.CrossRefGoogle ScholarPubMed
CHEEK, M. & JEBB, M. 2001. Nepenthaceae. Flora Malesiana. Publication Department of the National Herbarium Nederland, Leiden. 164 pp.Google Scholar
CLARKE, C. M. 1997. Nepenthes of Borneo. Natural History Publications (Borneo) Sdn. Bhd., Kota Kinabalu. 207 pp.Google Scholar
CLARKE, C. M. & KITCHING, R. L. 1993. The metazoan food webs from six Bornean Nepenthes species. Ecological Entomology 18:7–16.CrossRefGoogle Scholar
CLARKE, C. M. & KITCHING, R. L. 1995. Swimming ants and pitcher plants: a unique ant-plant interaction from Borneo. Journal of Tropical Ecology 11:589–602.CrossRefGoogle Scholar
CLARKE, C. M., BAUER, U., LEE, C. C., TUEN, A. A., REMBOLD, K. & MORAN, J. A. 2009. Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters 5:632–635.CrossRefGoogle Scholar
CRESSWELL, J. E. 2000. Resource input and the community structure of larval infaunas of an eastern tropical pitcher plant Nepenthes bicalcarata. Ecological Entomology 25:362–366.CrossRefGoogle Scholar
DEJEAN, A., SOLANO, P. J., AYROLES, J., CORBARA, B. & ORIVEL, J. 2005. Arboreal ants build traps to capture prey. Nature 434:973.CrossRefGoogle ScholarPubMed
GIUSTO, DI, 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 33:121–136.CrossRefGoogle Scholar
DI GIUSTO, B., BESSIÈRE, J.-M., GUÉROULT, 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 98:845–856.CrossRefGoogle Scholar
ELLISON, A. M. & GOTELLI, N. J. 2001. Evolutionary ecology of carnivorous plants. Trends in Ecology and Evolution 16:623–629.CrossRefGoogle Scholar
FEDERLE, W., MASCHWITZ, U. & HÖLLDOBLER, B. 2002. Pruning of host plant neighbours as defence against enemy ant invasions: Crematogaster ant partners of Macaranga protected by “wax barriers” prune less than their congeners. Oecologia 132:264–270.CrossRefGoogle ScholarPubMed
GAUME, L. & DI GIUSTO, B. 2009. Adaptive significance and ontogenetic variability of the waxy zone in Nepenthes rafflesiana. Annals of Botany 104:1281–1291.CrossRefGoogle ScholarPubMed
GAUME, L. & FORTERRE, Y. 2007. A viscoelastic deadly fluid in carnivorous pitcher plants. PLoS ONE 2:e1185.CrossRefGoogle ScholarPubMed
GAUME, L., GORB, S. & ROWE, N. 2002. Function of epidermal surfaces in the trapping efficiency of Nepenthes alata pitchers. New Phytologist 156:479–489.CrossRefGoogle ScholarPubMed
GAUME, L., ZACHARIAS, M., GROSBOIS, V. & BORGES, R. 2005. The fitness consequences of bearing domatia and having the right ant partner: experiments with protective and non-protective ants in a semi-myrmecophyte. Oecologia 145:76–86.CrossRefGoogle Scholar
GAUME, L., SHENOY, M., ZACHARIAS, M. & BORGES, R. M. 2006. Co-existence of ants and an arboreal earthworm in a myrmecophyte of the Indian Western Ghats: anti-predation effect of the earthworm mucus. Journal of Tropical Ecology 22:341–344.CrossRefGoogle Scholar
HÖLLDOBLER, B. & WILSON, E. O. 1990. The ants. Belknap Press, Cambridge. 732 pp.CrossRefGoogle Scholar
HUXLEY, C. R. 1978. The ant-plants Myrmecodia and Hydnophytum (Rubiaceae), and the relationships between their morphology, ant occupants, physiology and ecology.New Phytologist 80:231–268.CrossRefGoogle Scholar
JANZEN, D. H. 1974. Tropical blackwater rivers, animals and mast fruiting by the Dipterocarpaceae. Biotropica 6:69–103.CrossRefGoogle Scholar
JOLIVET, P. 1986. Les fourmis et les plantes, un exemple de coévolution. Boubée, Paris. 254 pp.Google Scholar
JONES, D. T. & GATHORNE-HARDY, F. 1995. Foraging activity of the processional termite, Hospitalitermes hospitalis (Termitidae, Nasutitermitinae) in the rain forest of Brunei, North-West Borneo. Insectes Sociaux 42:359–369.CrossRefGoogle Scholar
JUNIPER, B. E., ROBINS, R. J. & JOEL, D. 1989. The carnivorous plants. Academic Press, London. 353 pp.Google Scholar
MCKEY, D., GAUME, L., BROUAT, C., DI GIUSTO, B., PASCAL, L., DEBOUT, G., DALECKY, A. & HEIL, M. 2005. The trophic structure of tropical ant-plant-herbivore interactions: community consequences and coevolutionary dynamics. Pp. 386–413 in Hartley, S., Burslem, D. & Pinard, M. (eds.). Biotic interactions in the tropics. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
MCPHERSON, S. 2009. Pitcher plants of the Old World. Redfern Natural History Productions, Poole. 1399 pp.Google Scholar
MERBACH, M. A., ZIZKA, G., FIALA, B., MERBACH, D. & MASCHWITZ, U. 1999. Giant nectaries in the peristome thorns of the pitcher plant Nepenthes bicalcarata Hooker f. (Nepenthaceae): anatomy and functional aspects. Ecotropica 5:45–50.Google Scholar
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 415:36–37.CrossRefGoogle ScholarPubMed
MERBACH, M. A., ZIZKA, G., FIALA, B., MERBACH, D. J., BOOTH, W. E. & MASCHWITZ, U. 2007. Why a carnivorous plant cooperates with an ant-selective defense against pitcher-destroying weevils in the myrmecophytic pitcher plant Nepenthes bicalcarata Hook. f. Ecotropica 13:45–56.Google Scholar
MORAN, J. A. 1996. Pitcher dimorphism, prey composition and the mechanism of prey attraction in the pitcher plant Nepenthes rafflesiana in Borneo. Journal of Ecology 84:515–525.CrossRefGoogle Scholar
MORAN, J. A., MERBACH, M. A., LIVINGSTON, N. J., CLARKE, C. M. & BOOTH, W. E. 2001. Termite prey specialization in the pitcher plant Nepenthes albomarginata – evidence from stable isotope analysis. Annals of Botany 88:307–311.CrossRefGoogle Scholar
MORAN, J. A., CLARKE, C. M. & HAWKINS, B. J. 2003. From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria. International Journal of Plant Sciences 164:635–639.CrossRefGoogle Scholar
MORAN, J. A., HAWKINS, B. J., GOWEN, B. E. & ROBBINS, S. L. 2010. Ion fluxes across the pitcher walls of three Bornean Nepenthes pitcher plant species: flux rates and gland distribution patterns reflect nitrogen sequestration strategies. Journal of Experimental Botany 61:1365–1374.CrossRefGoogle Scholar
SCHULTZE, W., SCHULTZE, E. D., PATE, J. S. & GILLISON, A. N. 1997. The nitrogen supply from soils and insects during growth of the pitcher plants Nepenthes mirabilis, Cephalotus follicularis and Darlingtonia californica. Oecologia 112:464–471.CrossRefGoogle Scholar
SOLANO, P.-J. & DEJEAN, A. 2004. Ant-fed plants: comparison between three geophytic myrmecophytes. Biological Journal of the Linnean Society 83:433–439.CrossRefGoogle Scholar
THOMPSON, J. N. 1981. Reversed animal–plant interactions: the evolution of insectivorous and ant-fed plants. Biological Journal of the Linnean Society 16:147–155.CrossRefGoogle Scholar
TRESEDER, K. K., DAVIDSON, D. W. & EHLERINGER, J. R. 1995. Absorption of ant-provided carbon dioxide and nitrogen by a tropical epiphyte. Nature 375:137–139.CrossRefGoogle Scholar