Skip to main content
Log in

Change in biomass of symbiotic ants throughout the ontogeny of a myrmecophyte, Macaranga beccariana (Euphorbiaceae)

Journal of Plant Research Aims and scope Submit manuscript

Abstract

Macaranga myrmecophytes (ant-plants) provide their partner symbiotic ants (plant-ants) with food bodies as their main food, and they are protected by the plant-ants from herbivores. The amount of resource allocated to food bodies determines the plant-ant colony size and consequently determines the intensity of ant defense (anti-herbivore defense by plant-ants). As constraints in resource allocation change as plants grow, the plant-ant colony size is hypothesized to change with the ontogenesis of Macaranga myrmecophyte. To determine the ontogenetic change in the relative size of the plant-ant colony, we measured the dry weights of the whole plant-ant colony and all of the aboveground parts of trees at various ontogenetic stages for a myrmecophytic species (Macaranga beccariana) in a Bornean lowland tropical rain forest. Ant biomass increased as plant biomass increased. However, the rate of increase gradually declined, and the ant biomass appeared to reach a ceiling once trees began to branch. The ant/plant biomass ratio consistently decreased as plant biomass increased, with the rate of decrease gradually accelerating. We infer that the ontogenetic reduction in ant/plant biomass ratio is caused by an ontogenetic change in resource allocation to food rewards for ants related to the physiological changes accompanying the beginning of branching.

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

Access this article

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

Similar content being viewed by others

References

  • Ashton PS, Hall P (1992) Comparisons of structure among mixed dipterocarp forests of north-western Borneo. J Ecol 80:459–481

    Article  Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448

    Article  PubMed  Google Scholar 

  • Davidson DW, Fisher BL (1991) Symbiosis of ants with Cecropia as a function of light regime. In: Huxley CR, Cutler DF (eds) Ant-plant interactions. Oxford University Press, Oxford, pp 289–309

    Google Scholar 

  • Davidson DW, McKey D (1993) The evolutionary ecology of symbiotic ant-plant relationships. J Hymenopt Res 2:13–83

    Google Scholar 

  • Davies SJ (2001) Systematics of Macaranga sects. Pachystemon and Pruinosae (Euphorbiaceae). Harv Pap Bot 6:371–448

    Google Scholar 

  • Davies SJ, Ashton PS (1999) Phenology and fecundity in 11 sympatric pioneer species of Macaranga (Euphorbiaceae) in Borneo. Am J Bot 86:1786–1795

    Article  PubMed  CAS  Google Scholar 

  • Davies SJ, Palmiotto PA, Ashton PS, Lee HS, Lafrankie JV (1998) Comparative ecology of 11 sympatric species of Macaranga in Borneo: tree distribution in relation to horizontal and vertical resource heterogeneity. J Ecol 86:662–673

    Article  Google Scholar 

  • Fiala B, Maschwitz U (1990) Studies on the South East Asian ant-plant association Crematogaster borneensis/Macaranga: adaptations of the ant partner. Insect Soc 37:212–231

    Article  Google Scholar 

  • Fiala B, Maschwitz U (1992a) Domatia as most important adaptations in the evolution of myrmecophytes in the paleotropical tree genus Macaranga (Euphorbiaceae). Plant Syst Evol 180:53–64

    Article  Google Scholar 

  • Fiala B, Maschwitz U (1992b) Food bodies and their significance for obligate ant-association in the tree genus Macaranga (Euphorbiaceae). Bot J Linn Soc 110:61–75

    Article  Google Scholar 

  • Fiala B, Maschwitz U, Pong TY, Helbig AJ (1989) Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79:463–470

    Article  Google Scholar 

  • Folgarait PJ, Davidson DW (1994) Antiherbivore defenses of myrmecophytic Cecropia under different light regimes. Oikos 71:305–320

    Article  Google Scholar 

  • Folgarait PJ, Davidson DW (1995) Myrmecophytic Cecropia: antiherbivore defenses under different nutrient treatments. Oecologia 104:189–206

    Article  Google Scholar 

  • Gaume L, McKey D, Terrin S (1998) Ant-plant-homopteran mutualism: how the third partner affects the interaction between a plant-specialist ant and its myrmecophyte host. Proc R Soc Lond B 265:569–575

    Article  Google Scholar 

  • Hashimoto Y, Yamane S, Itioka T (1997) A preliminary study on dietary habits of ants in a Bornean rain forest. Jpn J Entomol 65:688–695

    Google Scholar 

  • Hatada A, Itioka T, Yamaoka R, Itino T (2002) Carbon and nitrogen contents of food bodies in three myrmecophytic species of Macaranga: implications for antiherbivore defense mechanisms. J Plant Res 115:179–184

    Article  PubMed  Google Scholar 

  • Heil M, Fiala B, Linsenmair KE, Zotz G, Menke P, Maschwitz U (1997) Food body production in Macaranga triloba (Euphorbiaceae): a plant investment in anti-herbivore defense via symbiotic ant partners. J Ecol 85:847–861

    Article  Google Scholar 

  • Heil M, Fiala B, Kaiser W, Linsenmair KE (1998) Chemical contents of Macaranga food bodies: adaptations to their role in ant attraction and nutrition. Funct Ecol 12:118–122

    Article  Google Scholar 

  • Heil M, Hilpert A, Fiala B, Linsenmair KE (2001) Nutrient availability and indirect (biotic) defense in a Malaysian ant-plant. Oecologia 126:404–408

    Article  Google Scholar 

  • Heil M, Feil D, Hilpert A, Linsenmair KE (2004) Spatiotemporal patterns in indirect defence of a South-East Asian ant-plant support the optimal defence hypothesis. J Trop Ecol 20:573–580

    Article  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Itino T, Itioka T, Hatada A, Hamid AA (2001) Effects of food rewards offered by ant-plant Macaranga on the colony size of ants. Ecol Res 16:775–786

    Article  Google Scholar 

  • Itioka T (2005) Diversity of anti-herbivore defenses in Macaranga. In: Roubik DW, Sakai S, Karim AAH (eds) Pollination ecology and the rain forest: sarawak studies. Springer, New York, pp 158–171

    Chapter  Google Scholar 

  • Itioka T, Nomura M, Inui Y, Itino T, Inoue T (2000) Difference in intensity of ant defense among three species of Macaranga myrmecophytes in a Southeast Asian dipterocarp forest. Biotropica 32:318–326

    Google Scholar 

  • Kato M, Inoue T, Hamid AA, Nagamitsu T, Merdek MB, Nona AR, Itino T, Yamane S, Yumoto T (1995) Seasonality and vertical structure of light-attracted insect communities in a dipterocarp forest in Sarawak. Res Popul Ecol 37:59–79

    Article  Google Scholar 

  • Kersch MF, Fonseca CR (2005) Abiotic factors and the conditional outcome of an ant-plant mutualism. Ecology 86:2117–2126

    Article  Google Scholar 

  • Linsenmair KE, Heil M, Kaiser WM, Fiala B, Koch T, Boland W (2001) Adaptations to biotic and abiotic stress: Macaranga-ant plants optimize investment in biotic defence. J Exp Bot 52:2057–2065

    Article  PubMed  CAS  Google Scholar 

  • Mori S, Yamaji K, Ishida A, Prokushkin SG, Masyagina OV, Hagihara A et al (2010) Mixed-power scaling of whole-plant respiration from seedlings to giant trees. Proc Natl Acad Sci USA 107:1447–1451

    Google Scholar 

  • Nomura M, Itioka T, Murase K (2001) Non-ant antiherbivore defenses before plant-ant colonization in Macaranga myrmecophytes. Popul Ecol 43:207–212

    Article  Google Scholar 

  • Nomura M, Hatada A, Itioka T (2011) Correlation between the leaf turnover rate and anti-herbivore defence strategy (balance between ant and non-ant defences) amongst ten species of Macaranga (Euphorbiaceae). Plant Ecol 212:143–155

    Article  Google Scholar 

  • Rehr SS, Feeny PP, Janzen DH (1973) Chemical defence in Central American non-ant-acacias. J Anim Ecol 42:405–416

    Article  Google Scholar 

  • Rocha CFD, Bergallo HG (1992) Bigger ant colonies reduce herbivory and herbivore residence time on leaves of an ant-plant: Azteca muelleri vs. Coelomera ruficornis on Cecropia pachystachya. Oecologia 91:249–252

    Article  Google Scholar 

  • Roubik DW, Sakai S, Karim AAH (eds) (2005) Pollination ecology and the rain forest: sarawak studies. Springer, New York

  • Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55

    Article  PubMed  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Traeger MD, Bruna EM (2006) Effects of plant age, experimental nutrient addition and ant occupancy on herbivory in a neotropical myrmecophyte. J Ecol 94:1156–1163

    Article  Google Scholar 

  • Weiner J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol Evolut Syst 6:207–215

    Article  Google Scholar 

  • Zhang DY, Jiang XH (2002) Size-dependent resource allocation and sex allocation in herbaceous perennial plants. J Evol Biol 15:74–83

    Article  Google Scholar 

Download references

Acknowledgments

We thank L. Chong, J. J. Kendawang and other staff members of the Forest Research Centre, Sarawak, and Forest Department of Sarawak for providing access to the study site as well as kind assistance. We are also grateful to T. Nakashizuka, M. Ichikawa, N. Yamamura and S. Sakai for supporting our research activities. This work was supported by Grants-in-Aid from the Japan Society for the Promotion of Science (JSPS) to T. I. (No. 17405006) and to C. H. as a JSPS Fellow and from the Research Institute for Humanity and Nature (project numbers 2-2, D-04).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chihiro Handa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Handa, C., Okubo, T., Yoneyama, A. et al. Change in biomass of symbiotic ants throughout the ontogeny of a myrmecophyte, Macaranga beccariana (Euphorbiaceae). J Plant Res 126, 73–79 (2013). https://doi.org/10.1007/s10265-012-0500-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-012-0500-z

Keywords

Navigation