Skip to main content
Log in

Intraspecific variation in the status of ant symbiosis on a myrmecophyte, Macaranga bancana, between primary and secondary forests in Borneo

  • Original Article
  • Published:
Population Ecology

Abstract

A tree species, Macaranga bancana , distributed in South East Asian tropics has a mutualistic relationship with specific symbiotic ant species, which defend the plant from herbivores. To examine the intraspecific variation in the status of the ant-plant symbiosis among microhabitats of different light conditions, we investigated the species composition of nesting ants and the herbivory damage on M. bancana saplings by field observations and sampling in primary and secondary forests in Sarawak. In addition, the effectiveness of non-ant (physical and chemical) defenses were estimated by feeding the larvae of a polyphagous lepidopteran with M. bancana leaves from saplings in the two types of forests. All saplings in the primary forest were colonized by two Crematogaster ant species that had been known to be the obligate symbionts of M. bancana, while in the secondary forest, about half of the saplings were occupied by several ant species that were not obligate symbionts. There was little herbivory damage on saplings colonized by the two Crematogaster symbiont ants in both forest types, while the saplings colonized by the other ant species suffered a 10–60% loss of leaf area. Larval mortality of the polyphagous lepidopteran Spodoptera litura was significantly higher when larvae fed on leaves of M. bancana saplings in the secondary forest than when fed on leaves of M. bancana saplings in the primary forest. These results suggest that the symbiosis between ants and M. bancana is looser and the non-ant-defenses are stronger in secondary forests, where light is more intense, than in primary forests.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agrawal AA, Rutter MT (1998) Dynamic anti-herbivore defense in ant-plants: the role of induced responses. Oikos 83:227–236

    Google Scholar 

  • Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, Cambridge

  • Begon M, Harper JL, Townsend CR (1996) Ecology, 3rd edn. Blackwell Science, Oxford

  • Buckley RC (ed) (1982) Ant-plant interactions in Australia. Junk, The Hague

  • Chazdon RL (1986) Light variation and carbon gain in rain forest understorey palms. J Ecol 74:995–1012

    Google Scholar 

  • Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    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

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

    Google Scholar 

  • Davies SJ (1998) Photosynthesis of nine pioneer Macaranga species from Borneo in relation to life history. Ecology 79:2292–2308

    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 

  • Eck G, Fiala B, Linsenmair KE, Hashim RB, Proksch P (2001) Trade-off between chemical and biotic antiherbivore defense in the South East Asian plant genus Macaranga. J Chem Ecol 27:1979–1996

    Article  CAS  PubMed  Google Scholar 

  • Fiala B, Maschwitz U (1991) Extrafloral nectaries in the genus Macaranga (Euphorbiaceae) in Malaysia: comparative studies of their possible significance as predispositions for myrmecophytism. Biol J Linn Soc 44:287–306

    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

    Google Scholar 

  • Fiala B, Grunsky H, Maschwitz U, Linsenmair KE (1994) Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association. Oecologia 97:186–192

    Google Scholar 

  • Fiala B, Jakob A, Maschwitz U, Linsenmair KE (1999) Diversity, evolutionary specialization and geographic distribution of a mutualistic ant-plant complex: Macaranga and Crematogaster in South East Asia. Bot J Linn Soc 66:305–331

    Article  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Huxley CR, Cutler DF (eds) (1991) Ant-plant interactions. Oxford University Press, Oxford

  • Inoue T, Hamid AA (eds) (1994) Plant reproductive systems and animal seasonal dynamics: long-term study of dipterocarp forests in Sarawak. Center for Ecological Research, Kyoto University, Otsu

    Google Scholar 

  • Itino T, Itioka T (2001) Interspecific variation and ontogenetic change in antiherbivore defense in myrmecophytic Macaranga species. Ecol Res 16:765–774

    Article  Google Scholar 

  • Itino T, Davies SJ, Tada H, Hieda Y, Inoguchi M, Itioka T, Yamane S-K, Inoue T (2001) Co-speciation of ants and plants. Ecol Res 16:787–793

    Article  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 

  • Janzen DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249–275

    Google Scholar 

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

    Google Scholar 

  • Koricheva J, Larsson S, Haukioja E, Keinanen M (1998) Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos 83:212–226

    CAS  Google Scholar 

  • Larsson S, Wiren A, Lundgren L, Ericsson T (1986) Effects of light and nutrient stress on leaf phenolic chemistry in Salix dasyclados and susceptibility to Galerucella lineola (Coleoptera). Oikos 47:205–210

    CAS  Google Scholar 

  • Longino JT (1989) Geographic variation and community structure in an ant-plant mutualism Azteca and Cecropia in Costa Rica. Biotropica 21:126–132

    Google Scholar 

  • Maschwitz U, Fiala B, Davies SJ, Linsenmair KE (1996) A South-East Asian myrmecophyte with two alternative inhabitants: Camponotus or Crematogaster as partners of Macaranga lamellata. Ecotropica 2:29–40

    Google Scholar 

  • McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320

    Article  Google Scholar 

  • McKey D (1984) Interaction of the ant-plant Leonardoxa africana (Caesalpiniaceae) with its obligate inhabitants in a rainforest in Cameroon. Biotropica 16:81–99

    Google Scholar 

  • McKey D, Davidson DW (1993) Ant-plant symbioses in Africa and the neotropics: history, biogeography, and diversity. In: Goldblatt P (ed) Biological relationships between Africa and South America. Yale University Press, New Haven, Connecticut, pp 567–606

  • Nichols-Orians CM (1991a) Environmentally induced differences in plant traits: consequences for susceptibility to a leaf-cutter ant. Ecology 72:1609–1623

    Google Scholar 

  • Nichols-Orians CM (1991b) The effects of light on foliar chemistry, growth and susceptibility of seedlings of a canopy tree to an attine ant. Oecologia 86:552–560

    Google Scholar 

  • Nicotra AB, Chazdon RL, Iriarte SVB (1999) Spatial heterogeneity of light and woody seedling regeneration in tropical wet forests. Ecology 80:1908–1926

    Google Scholar 

  • Nomura M, Itioka T (2002) Effects of synthesized tannin on the growth and survival of a generalist herbivorous insect, the common cutworm, Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Appl Entomol Zool 37:285–289

    Google Scholar 

  • Nomura M, Itioka T, Itino T (2000) Variations in abiotic defense among myrmecophytic and non-myrmecophytic species of Macaranga in a Bornean dipterocarp forest. Ecol Res 15:1–11

    Article  Google Scholar 

  • Okamoto D, Okada S (1968) Studies on the tobacco cutworm, Spodoptera litura , Fabricius, as an insect pest of the forage crop (in Japanese). Bull Chugoku Natl Agric Exp Stat Ser 2:111–144

    Google Scholar 

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

    Google Scholar 

  • Seemann JR, Sharkey TD, Wang J, Osmond CB (1987) Environmental effects on photosynthesis, nitrogen-use efficiency, and metabolite pools in leaves of sun and shade plants. Plant Physiol 84:796–802

    CAS  Google Scholar 

  • Siemens DH, Garner SH, Mitchell-Olds T, Callaway RM (2002) Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 83:505–517

    Google Scholar 

  • Simms EL (1992) Costs of plant resistance to herbivory. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. The University of Chicago Press, Chicago, pp 392–425

  • Whitmore TC (1969) First thoughts on species evolution in Malayan Macaranga (Studies in Macaranga III). Biol J Linn Soc 1:223–231

    Google Scholar 

  • Whitmore TC (1975) Macaranga. In: Airy Shaw HK (ed) The Euphorbiaceae of Borneo. Kew Bull Add Ser 4:140–159

    Google Scholar 

  • Yu DW, Davidson DW (1997) Experimental studies of species-specificity in Cecropia -ant relationships. Ecol Monogr 67:273–294

    Google Scholar 

  • Zangerl AR, Bazzaz FA (1992) Theory and pattern in plant defense allocation. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. The University of Chicago Press, Chicago, pp 363–391

Download references

Acknowledgements

We thank Hua Seng Lee, Tohru Nakashizuka and Takayuki Ohgushi for providing support and assistance for this study. We also thank Abang A. Hamid and Sarkawi M. Umar and the staff of Entomological Unit of Forest Research Centre, Sarawak for providing research facilities. We are grateful to Takao Itino and Aya Hatada for fruitful discussions. Diane W. Davidson is acknowledged for valuable comments on an earlier draft of the manuscript. Thanks are also due to Tomoaki Ichie and Michiko Nakagawa for help in the field. This work was supported partly by the Japan Ministry of Education, Culture, Sports, Science and Technology for International Scientific Research (#10041163) and by CREST of JST (Japan Science and Technology Corporation).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takao Itioka.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Murase, K., Itioka, T., Nomura, M. et al. Intraspecific variation in the status of ant symbiosis on a myrmecophyte, Macaranga bancana, between primary and secondary forests in Borneo. Popul Ecol 45, 221–226 (2003). https://doi.org/10.1007/s10144-003-0158-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10144-003-0158-4

Keywords

Navigation