Skip to main content
SpringerLink
Log in

Are ant feces nutrients for plants? A metabolomics approach to elucidate the nutritional effects on plants hosting weaver ants

  • Original Article
  • Published:
Metabolomics Aims and scope Submit manuscript

Abstract

Weaver ants (genus Oecophylla) are tropical carnivorous ant species living in high numbers in the canopies of trees. The ants excrete copious amounts of fecal matter on leaf surfaces, and these feces may provide nutrients to host trees. This hypothesis is supported by studies of ant-plant interactions involving other ant species that have demonstrated the transfer of nutrients from ants to plants. In this 7-months study, a GC–MS-based metabolomics approach along with an analysis of total nitrogen and carbon levels was used to study metabolic changes in ant-hosting Coffea arabica plants compared with control plants. The results showed elevated levels of total nitrogen, amino acids, fatty acids, caffeine, and secondary metabolites of the phenylpropanoid pathway in leaves from ant-hosting plants. Minor effects were observed for sugars, whereas little or no effect was observed for organic acids, despite the fact that lower levels of total carbon were found in ant-hosting plants. The increased levels of total nitrogen, amino acids, fatty acids and caffeine and the decreased total carbon were consistent with changes observed in plants grown with an increased supply of nitrogen-containing nutrients. The up-regulation of the phenylpropanoid pathway could indicate biotic stress and/or nutrient deficiency. However, because nutrient deficiency was contradicted by the remaining results, this pathway up-regulation was ascribed to biotic stress caused by the physical presence of the weaver ants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amtmann, A., & Armengaud, P. (2009). Effects of N, P, K and S on metabolism: New knowledge gained from multi-level analysis. Current Opinion in Plant Biology, 12(3), 275–283.

    Article  CAS  PubMed  Google Scholar 

  • Barker, M., & Rayens, W. (2003). Partial least squares for discrimination. Journal of Chemometrics, 17(3), 166–173.

    Article  CAS  Google Scholar 

  • Barzman, M. S., Mills, N. J., & Nguyen Thi Thu, C. (1996). Traditional knowledge and rationale for weaver ant husbandry in the Mekong delta of Vietnam. Agriculture and Human Values, 13(4), 2–9.

    Article  Google Scholar 

  • Bennett, R. N., & Wallsgrove, R. M. (1994). Secondary metabolites in plant defence mechanisms. New Phytologist, 127(4), 617–633.

    Article  CAS  Google Scholar 

  • Bondada, B. R., Syvertsen, J. P., & Albrigo, L. G. (2001). Urea nitrogen uptake by citrus leaves. HortScience, 36(6), 1061–1065.

    CAS  Google Scholar 

  • Bradley, D. P., Morgan, M. A., & Otoole, P. (1989). Uptake and apparent utilization of urea and ammonium nitrate in wheat seedlings. Fertilizer Research, 20(1), 41–49.

    Article  CAS  Google Scholar 

  • Davidson, D. W. (1997). The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biological Journal of the Linnean Society, 61(2), 153–181.

    Article  Google Scholar 

  • Diaz, C., Saliba-Colombani, V., Loudet, O., Belluomo, P., Moreau, L., Daniel-Vedele, F., et al. (2006). Leaf yellowing and anthocyanin accumulation are two genetically independent strategies in response to nitrogen limitation in Arabidopsis thaliana. Plant and Cell Physiology, 47(1), 74–83.

    Article  CAS  PubMed  Google Scholar 

  • Dixon, R. A., & Paiva, N. L. (1995). Stress-induced phenylpropanoid metabolism. Plant Cell, 7(7), 1085–1097.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dong, S. F., Cheng, L. L., Scagel, C. F., & Fuchigami, L. H. (2002). Nitrogen absorption, translocation and distribution from urea applied in autumn to leaves of young potted apple (Malus domestica) trees. Tree Physiology, 22(18), 1305–1310.

    Article  CAS  PubMed  Google Scholar 

  • Emam, Y., & Moaied, G. R. (1998). The effects of foliar spray of urea at grain filling period on grain yield and grain protein content of winter wheat, Triticum aestivum L. Crop Research (Hisar), 15(2–3), 135–139.

    Google Scholar 

  • Fiehn, O. (2014). Metabolomics Fiehn Lab—Fiehn Databases Home Page. http://fiehnlab.ucdavis.edu/db/. Accessed January 7.

  • Fiehn, O., Wohlgemuth, G., & Scholz, M. (2005). Setup and annotation of metabolomic experiments by integrating biological and mass spectrometric metadata. In B. Ludascher & L. Raschid (Eds.), Data Integration in the Life Sciences (Vol. 3615, pp. 224–239). Berlin: Springer.

    Chapter  Google Scholar 

  • Fiehn, O., Wohlgemuth, G., Scholz, M., Kind, T., Lee, D. Y., Lu, Y., et al. (2008). Quality control for plant metabolomics: reporting MSI-compliant studies. Plant Journal, 53(4), 691–704.

    Article  CAS  PubMed  Google Scholar 

  • Fischer, R. C., Wanek, W., Richter, A., & Mayer, V. (2003). Do ants feed plants? A N-15 labelling study of nitrogen fluxes from ants to plants in the mutualism of Pheidole and Piper. Journal of Ecology, 91(1), 126–134.

    Article  Google Scholar 

  • Foito, A., Byrne, S. L., Hackett, C. A., Hancock, R. D., Stewart, D., & Barth, S. (2013). Short-term response in leaf metabolism of perennial ryegrass (Lolium perenne) to alterations in nitrogen supply. Metabolomics, 9(1), 145–156.

    Article  CAS  Google Scholar 

  • Folgarait, P. J. (1998). Ant biodiversity and its relationship to ecosystem functioning: A review. Biodiversity and Conservation, 7(9), 1221–1244.

    Article  Google Scholar 

  • Foyer, C. H., Noctor, G., & van Emden, H. F. (2007). An evaluation of the costs of making specific secondary metabolites: Does the yield penalty incurred by host plant resistance to insects result from competition for resources? International Journal of Pest Management, 53(3), 175–182.

    Article  CAS  Google Scholar 

  • Foyer, C. H., Parry, M., & Noctor, G. (2003). Markers and signals associated with nitrogen assimilation in higher plants. Journal of Experimental Botany, 54(382), 585–593.

    Article  CAS  PubMed  Google Scholar 

  • Furuya, S., & Umemiya, Y. (2002). The influence of chemical forms on foliar-applied nitrogen absorption for peach trees. In M. Tagliavini, M. Toselli, L. Bertschinger, D. Neilsen, & M. Thalheimer (Eds.), Proceedings of the International Symposium on Foliar Nutrition of Perennial Fruit Plants (pp. 97–103, Vol. 594): International Society for Horticultural Science.

  • Gislum, R., Boelt, B., & Zhang, X. (2009). The use of linear mixed models for analysis of repeated measurements applied to water-soluble carbohydrates in perennial ryegrass for seed production. Acta Agriculturae Scandinavica Section B-Soil and Plant Science, 59(2), 151–156.

    Article  CAS  Google Scholar 

  • Gonthier, D. J., Witter, J. D., Spongberg, A. L., & Philpott, S. M. (2011). Effect of nitrogen fertilization on caffeine production in coffee (Coffea arabica). Chemoecology, 21(3), 123–130.

    Article  CAS  Google Scholar 

  • Hermans, C., Hammond, J. P., White, P. J., & Verbruggen, N. (2006). How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science, 11(12), 610–617.

    Article  CAS  PubMed  Google Scholar 

  • Herms, D. A., & Mattson, W. J. (1992). The dilemma of plants: To grow or defend. Quarterly Review of Biology, 67(3), 283–335.

    Article  Google Scholar 

  • Holldobler, B., & Wilson, E. O. (1977). Weaver ants—Social establishment and maintenance of territory. Science, 195(4281), 900–902.

    Article  CAS  PubMed  Google Scholar 

  • Holldobler, B., & Wilson, E. O. (1994). Journey to the ants, a story of scientific exploration (Vol. 2). Cambridge: Harvard University Press.

    Google Scholar 

  • Huang, H. T., & Yang, P. (1987). The ancient cultured citrus ant. BioScience, 37(9), 665–671.

    Article  Google Scholar 

  • Kerchev, P. I., Fenton, B., Foyer, C. H., & Hancock, R. D. (2012). Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant, Cell and Environment, 35(2), 441–453.

    Article  CAS  PubMed  Google Scholar 

  • Kind, T., Wohlgemuth, G., Lee, D. Y., Lu, Y., Palazoglu, M., Shahbaz, S., et al. (2009). FiehnLib: Mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Analytical Chemistry, 81(24), 10038–10048.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lam, H. M., Coschigano, K. T., Oliveira, I. C., MeloOliveira, R., & Coruzzi, G. M. (1996). The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology, 47, 569–593.

    Article  CAS  PubMed  Google Scholar 

  • Lemaitre, T., Gaufichon, L., Boutet-Mercey, S., Christ, A., & Masclaux-Daubresse, C. (2008). Enzymatic and metabolic diagnostic of nitrogen deficiency in Arabidopsis thaliana Wassileskija accession. Plant and Cell Physiology, 49(7), 1056–1065.

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Bucio, J., Nieto-Jacobo, M. F., Ramirez-Rodriguez, V., & Herrera-Estrella, L. (2000). Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Science, 160(1), 1–13.

    Article  CAS  PubMed  Google Scholar 

  • Margna, U. (1977). Control at the level of substrate supply—alternative in regulation of phenylpropanoid accumulation in plant cells. Phytochemistry, 16(4), 419–426.

    Article  CAS  Google Scholar 

  • Mazzafera, P. (1999). Mineral nutrition and caffeine content in coffee leaves. Bragantia, 58(2), 387–391.

    Article  CAS  Google Scholar 

  • Merigout, P., Lelandais, M., Bitton, F., Renou, J.-P., Briand, X., Meyer, C., et al. (2008). Physiological and transcriptomic aspects of urea uptake and assimilation in Arabidopsis plants. Plant Physiology, 147(3), 1225–1238.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Montagnon, C., Guyot, B., Cilas, C., & Leroy, T. (1998). Genetic parameters of several biochemical compounds from green coffee. Coffea canephora. Plant Breeding, 117(6), 576–578.

    Article  CAS  Google Scholar 

  • Moraes, F. R. P. (1981). Adubação do cafeeiro. Macronutrientes e adubação orgânica. In E. Malavolta, T. Yamada, & J. A. Guidolin (Eds.), Nutrição e adubação de cafeeiro (pp. 77–89). Piracicaba: Instituto Internacional de Potassa.

    Google Scholar 

  • Nestby, R., & Tagliavini, M. (2005). Foliar uptake and partitioning of urea-N by strawberry plants as affected by timing of supply and plant N status. Journal of Horticultural Science & Biotechnology, 80(2), 272–275.

    CAS  Google Scholar 

  • Noctor, G., Novitskaya, L., Lea, P. J., & Foyer, C. H. (2002). Co-ordination of leaf minor amino acid contents in crop species: significance and interpretation. Journal of Experimental Botany, 53(370), 939–945.

    Article  CAS  PubMed  Google Scholar 

  • Offenberg, J. (2007). The distribution of weaver ant pheromones on host trees. Insectes Sociaux, 54(3), 248–250.

    Article  Google Scholar 

  • Peng, R. K., & Christian, K. (2005). Integrated pest management in mango orchards in the Northern Territory Australia, using the weaver ant, Oecophylla smaragidina, (Hymenoptera : Formicidae) as a key element. International Journal of Pest Management, 51(2), 149–155.

    Article  Google Scholar 

  • Peng, M., Hudson, D., Schofield, A., Tsao, R., Yang, R., Gu, H., et al. (2008). Adaptation of Arabidopsis to nitrogen limitation involves induction of anthocyanin synthesis which is controlled by the NLA gene. Journal of Experimental Botany, 59(11), 2933–2944.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pompelli, M. F., Martins, S. C. V., Antunes, W. C., Chaves, A. R. M., & DaMatta, F. M. (2010). Photosynthesis and photoprotection in coffee leaves is affected by nitrogen and light availabilities in winter conditions. Journal of Plant Physiology, 167(13), 1052–1060.

    Article  CAS  PubMed  Google Scholar 

  • Raju, K. I., Venkataramanan, D., & Vasudeva, N. (1984). Variations of caffeine, total nitrogen and dry matter in the leaves of arabica and robusta coffee. Journal of Coffee Research, 14(1), 38–42.

    CAS  Google Scholar 

  • Ramakrishna, A., & Ravishankar, G. A. (2011). Influence of abiotic stress signals on secondary metabolites in plants. Plant signaling & behavior, 6(11), 1720–1731.

    Article  CAS  Google Scholar 

  • Ramalho, J. C., Campos, P. S., Teixeira, M., & Nunes, M. A. (1998). Nitrogen dependent changes in antioxidant system and in fatty acid composition of chloroplast membranes from Coffea arabica L. plants submitted to high irradiance. Plant Science, 135(2), 115–124.

    Article  CAS  Google Scholar 

  • Rasmussen, S., Parsons, A. J., Fraser, K., Xue, H., & Newman, J. A. (2008). Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiology, 146(3), 1440–1453.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raven, J. A., & Wollenweber, B. (1992). A comparison between ammonium and nitrate as nitrogen sources for photolithotrophs. New Phytologist, 121(1), 19–32.

    Article  CAS  Google Scholar 

  • Readman, R. J., Kettlewell, P. S., & Beckwith, C. P. (2002). Effects of spray application of urea fertilizer at stem extension on winter wheat yield. Journal of Agricultural Science, 139, 1–10.

    CAS  Google Scholar 

  • Rosecrance, R. C., Johnson, R. S., & Weinbaum, S. A. (1998). Foliar uptake of urea-N by nectarine leaves: A reassessment. HortScience, 33(1), 158.

    CAS  Google Scholar 

  • Scheible, W. R., Morcuende, R., Czechowski, T., Fritz, C., Osuna, D., Palacios-Rojas, N., et al. (2004). Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiology, 136(1), 2483–2499.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schlueter, U., Mascher, M., Colmsee, C., Scholz, U., Braeutigam, A., Fahnenstich, H., et al. (2012). Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis. Plant Physiology, 160(3), 1384–1406.

    Article  CAS  Google Scholar 

  • Solecka, D. (1997). Role of phenylpropanoid compounds in plant responses to different stress factors. Acta Physiologiae Plantarum, 19(3), 257–268.

    Article  CAS  Google Scholar 

  • Stiegler, J. C., Richardson, M. D., Karcher, D. E., Roberts, T. L., & Norman, R. J. (2013). Foliar absorption of various inorganic and organic nitrogen sources by creeping bentgrass. Crop Science, 53(3), 1148–1152.

    Article  CAS  Google Scholar 

  • Tegeder, M. (2014). Transporters involved in source to sink partitioning of amino acids and ureides: Opportunities for crop improvement. Journal of Experimental Botany, 65(7), 1865–1878.

    Article  CAS  PubMed  Google Scholar 

  • Toselli, M., Thalheimer, M., & Tagliavini, M. (2004). Leaf uptake and subsequent partitioning of urea-N as affected by the concentration and volume of spray solution and by the shoot leaf position in apple (Malus domestica) trees. Journal of Horticultural Science & Biotechnology, 79(1), 97–100.

    Google 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(6527), 137–139.

    Article  CAS  Google Scholar 

  • Urbanczyk-Wochniak, E., & Fernie, A. R. (2005). Metabolic profiling reveals altered nitrogen nutrient regimes have diverse effects on the metabolism of hydroponically-grown tomato (Solanum lycopersicum) plants. Journal of Experimental Botany, 56(410), 309–321.

    Article  CAS  PubMed  Google Scholar 

  • Van Beusichem, M. L., & Neeteson, J. J. (1982). Urea nutrition of young maize and sugar-beet plants with emphasis on ionic balance and vascular transport of nitrogenous compounds. Netherlands Journal of Agricultural Science, 30(4), 317–330.

    Google Scholar 

  • van Dam, N. M. (2009). How plants cope with biotic interactions. Plant Biology, 11(1), 1–5.

    Article  PubMed  Google Scholar 

  • Van Mele, P. (2008). A historical review of research on the weaver ant Oecophylla in biological control. Agricultural and Forest Entomology, 10(1), 13–22.

    Google Scholar 

  • Vasilas, B. L., Legg, J. O., & Wolf, D. C. (1980). Foliar fertilization of soybeans—absorption and translocation of N-15 labeled urea. Agronomy Journal, 72(2), 271–275.

    Article  CAS  Google Scholar 

  • Wagner, D., & Nicklen, E. F. (2010). Ant nest location, soil nutrients and nutrient uptake by ant-associated plants: does extrafloral nectar attract ant nests and thereby enhance plant nutrition? Journal of Ecology, 98(3), 614–624.

    Article  Google Scholar 

  • Westerhuis, J. A., Hoefsloot, H. C. J., Smit, S., Vis, D. J., Smilde, A. K., van Velzen, E. J. J., et al. (2008). Assessment of PLSDA cross validation. Metabolomics, 4(1), 81–89.

    Article  CAS  Google Scholar 

  • Wink, M. (2003). Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry, 64(1), 3–19.

    Article  CAS  PubMed  Google Scholar 

  • Witte, C. P. (2011). Urea metabolism in plants. Plant Science, 180(3), 431–438.

    Article  CAS  PubMed  Google Scholar 

  • Wojtusiak, J., Godzinska, E. J., & Dejean, A. (1995). Capture and retrieval of very large prey by workers of the African weaver ant, Oecophylla longinoda (Latreille 1802). Tropical Zoology, 8(2), 309–318.

    Article  Google Scholar 

  • Wollenweber, B., & Raven, J. A. (1993). Implications of N aquisition from atmospheric NH3 for acid-base and cation-anion balance of Lolium perenne. Physiologia Plantarum, 89(3), 519–523.

    Article  CAS  Google Scholar 

  • Xia, J., Mandal, R., Sinelnikov, I. V., Broadhurst, D., & Wishart, D. S. (2012). MetaboAnalyst 2.0-a comprehensive server for metabolomic data analysis. Nucleic Acids Research, 40(W1), W127–W133.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xia, J., Psychogios, N., Young, N., & Wishart, D. S. (2009). MetaboAnalyst: A web server for metabolomic data analysis and interpretation. Nucleic Acids Research, 37, W652–W660.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zheng, X. Q., & Ashihara, H. (2004). Distribution, biosynthesis and function of purine and pyridine alkaloids in Coffea arabica seedlings. Plant Science, 166(3), 807–813.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was part of the project: “Adding value to ant-manure—from chemical interactions to ecosystem effects” (www.ant-manure.dk) funded by the Danish Council for Independent Research, Technology and Production Sciences.

Conflict of interest

None of the authors have any potential conflicts of interest.

Ethical statement

This article does not contain any studies with human or animal subjects.

Author information

Authors and Affiliations

  1. Department of Agroecology, Aarhus University, Forsøgsvej 1, 4200, Slagelse, Denmark

    Nanna H. Vidkjær, Bernd Wollenweber, René Gislum, Karl-Martin V. Jensen & Inge S. Fomsgaard

Authors
  1. Nanna H. Vidkjær
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bernd Wollenweber
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. René Gislum
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karl-Martin V. Jensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Inge S. Fomsgaard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Inge S. Fomsgaard.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 398 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vidkjær, N.H., Wollenweber, B., Gislum, R. et al. Are ant feces nutrients for plants? A metabolomics approach to elucidate the nutritional effects on plants hosting weaver ants. Metabolomics 11, 1013–1028 (2015). https://doi.org/10.1007/s11306-014-0757-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11306-014-0757-4

Keywords

Search

Navigation