Journal of Plant Research

, Volume 129, Issue 4, pp 591–601 | Cite as

Morphological and phylogenetic investigations for several cryptic ant-plants found in Callicarpa (Lamiaceae) from Borneo

  • Shota Nakashima
  • Emma Sarath
  • Hiroshi Okada
  • Kazune Ezaki
  • Dedy Darnaedi
  • Hirokazu Tsukaya
  • Akiko Soejima
Regular Paper


A tropical small tree, Callicarpa saccata, is known to have a symbiotic relationship with ants. It has sac-like structures at the base of the leaves that are inhabited by ants. No other species has been determined to be a myrmecophyte among the ca. 140 species of this genus. However, our recent field investigation discovered that two other species on Borneo (C. barbata and C. teneriflora) have hollow stems, which seem to be inhabited by ants. We observed the morphological features of these species in relation to their usage by ants, and became convinced that they are mymecophytic species. The molecular phylogenetic analyses using ITS and chloroplast regions suggest that C. saccata and C. teneriflora are closely related, but the differences in the myrmecophytic features of these species should be noted.


Ant-plant Borneo Callicarpa Coevolution Myrmecophyte Phylogeny 



The authors thank the Secretariat of Permission for Foreign Research, the Ministry of Research and Technology, Republic of Indonesia (RISTEK), who kindly gave permission for the field research in West Kalimantan, and the Indonesian Institute of Science (LIPI) and the Betung Kerihun National Park office, for kindly allowing this study to take place in Betung Kerihun National Park, West Kalimantan. We also thank Dr. Marlina Ardiyani and Mr. Ujang Hapid of Herbarium Bogoriense (BO), Mustarrudin, Suherman, Jon, Anong, Mazid, and Eddy for helping to conduct the botanical surveys during the expedition. We are grateful to Dr. Shingo Hosoishi of Kyushu University for doing elaborate identification of the ant specimens. A part of this study was supported by the Mitsubishi Foundation, MEXT/JSPS (Grants-in-Aid for Creative Scientific Research; Scientific Research on Innovative Areas) to H. T.


  1. Andersson S (2006) On the phylogeny of the genus Calceolaria (Calceolariaceae) as inferred from ITS and plastid matK sequences. Taxon 55:125–137CrossRefGoogle Scholar
  2. Ayala FJ, Wetterer JK, Longino JT, Hartl DL (1996) Molecular phylogeny of Azteca ants (Hymenoptera: Formicidae) and the colonization of Cecropia trees. Mol Phylogenet Evol 5:423–428CrossRefPubMedGoogle Scholar
  3. Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  4. Benson WW (1986) Amazon Ant-Plants. In: Pramce GT, Lovejoy TE (eds) Amazonia. Pargamon Press Ltd, Oxford, pp 239–266Google Scholar
  5. Bramley GLC (2009) The genus Callicarpa (Lamiaceae) on Borneo. Bot J Linean Soc 159:416–455CrossRefGoogle Scholar
  6. Cabrera M, Jaffe K (1994) A trophic mutualism between the myrmecophytic Melastomataceae Tococa guianensis Aublet and an Azteca ant species. Ecotropicos 7:1–10Google Scholar
  7. Chenuil A, McKey DB (1996) Molecular phylogenetic study of a myrmecophyte symbiosis: did Leonardoxa/ant associations diversify via cospeciation? Mol Phylogenet Evol 6:270–286CrossRefPubMedGoogle Scholar
  8. Chomicki G, Renner SS (2015) Phylogenetics and molecular clocks reveal the repeated evolution of ant-plants after the late Miocene in Africa and the early Miocene in Australasia and the Neotropics. New Phytol 207:411–424CrossRefPubMedGoogle Scholar
  9. Davidson DW, McKey D (1993) The evolutionary ecology of symbiotic ant-plant relationship. J Hymenop Res 2:13–83Google Scholar
  10. Dejean A, Mony R, Ngokam S, Djiéto C (1990) Arboreal nesting in various African ants. In: Veeresh GK, Mallik B, Viraktamath CA (eds) Social Insects and the Environment. Proceedings, 11th International Congress of the International Union for the Study of Social Insects. Oxford University Press, New Delhi, p 659Google Scholar
  11. Demesure B, Sodzi N, Petit RJ (1995) A set of universal primers for amplification of polymorphic noncoding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4:129–131CrossRefPubMedGoogle Scholar
  12. Doyle J, Doyle JL (1987) A rapid procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  13. Felsenstein J (1985) Confidence intervals on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefPubMedGoogle Scholar
  14. Fiala B, Maschwitz U, Pong TY, Helbig AJ (1989) Studies of a South Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79:463–470CrossRefPubMedGoogle Scholar
  15. 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 97:186–192CrossRefPubMedGoogle Scholar
  16. Fujikura U, Horiguchi G, Tsukaya H (2007) Dissection of enhanced cell expansion processes in leaves triggered by a defect in cell proliferation, with reference to roles of endoreduplication. Plant Cell Physiol 48:278–286CrossRefPubMedGoogle Scholar
  17. Harley RM, Atkins S, Budantsev AL, Cantino PD, Conn BJ, Grayer R, Harley MM, de Kok R, Krestovskaja T, Morales R, Paton AJ, Ryding O, Upson T (2004) Labiatae. In: Kadereit JW (ed) The Families and Genera of Vascular plants. VII. Flowering Plants: Dicotyledons: Lamiales (except Acanthaceae including Avicenniaceae). Springer, Berlin, pp 167–275Google Scholar
  18. Heckroth HP, Moog J, Jankal HI, Fialal B, Chung AYC (2004) Smilax borneensis (Smilacaceae), an unspecific climbing ant-plant from Borneo and myrmecophytic traits in other Asiatic Smilax species. Sandakania 14:33–50Google Scholar
  19. Herre EA, Windsor DM (1986) Nesting associations of wasps and ants on lowland Peruvian ant-plants. Psyche 93:321–330CrossRefGoogle Scholar
  20. Inui Y, Itioka T, Murase K, Yamaoka R, Itino T (2001) Chemical recognition of partner plant species by foundress ant queens in Macaranga-Crematogaster mymecophytism. J Chem Ecol 27:2029–2040CrossRefPubMedGoogle Scholar
  21. Itino T (2002) Ari to shokubutsu.—Kyo-sei no Shizenshi. In: Sugiura N, Ito F, Maeda Y (eds) Hachi to Ari no Shizenshi. Hokkaido University Press, Sapporo, pp 258–277 (in Japanese) Google Scholar
  22. Itino T, Davies SJ, Tada H, Hieda Y, Inoguchi M, Itioka T, Yamane S, Inoue T (2001) Cospeciation of ants and plants. Ecol Res 16:787–793CrossRefGoogle Scholar
  23. Itino T, Itioka T, Davies SJ (2003) Coadaptation and coevolution of Macaranga trees and their symbiotic ants. In: Kikuchi T, Azuma N, Higashi H (eds) Genes, Behaviors, and Evolution of Social Insects. Hokkaido University Press, Sapporo, pp 281–292Google Scholar
  24. Janka HL, Zizka G, Moog J, Maschwitz U (2000) Callicarpa saccata, eine Ameisenpflanze aus Borneo mit Blattdomatien und extrafloralen Nektarien—und das Verbreitungsrätsel von Blatttaschen—Ameisenpflanzen. Der Palmengarten 64:38–47Google Scholar
  25. Janzen DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20:248–275CrossRefGoogle Scholar
  26. Maschwitz U, Fiala B, Moog J, Saw LG (1991) Two new mymecophytic associations from the Malay Peninsula: ants of the genus Cladomyrma (Formicidae, Camponotinae) as partners of Saraca thaipingensis (Caesalpiniaceae) and Crypteronia griffithii (Crypteroniaceae). 1. Colony foundation and acquisition of trophobionts. Insects Sociaux 38:27–35CrossRefGoogle Scholar
  27. McKey D (1984) Interaction of the ant-plant Leonardoxa africana (Caesalpiniaceae) with its obligate inhabitants in a rainforest in Cameroon. Biotropica 16:81–99CrossRefGoogle Scholar
  28. McKey D (1991) Phylogenetic analysis of the evolution of a mutualism: Leonardoxa (Caesalpiniaceae) and its associated ants. In: Huxley CR, Cutler DF (eds) Ant-plant interactions. Oxford University Press, Oxford, pp 310–334Google Scholar
  29. Nkongmeneck BA (1985) Le Genre Cola au Cameroun. Annales de la Facultéde Sciences, Biologie-Biochimie, Université de Yaounde 3:5–27Google Scholar
  30. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biolog Centre, Uppsala University, 2Google Scholar
  31. Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  32. Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  33. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  34. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Axids Res 25:4876–4882CrossRefGoogle Scholar
  35. van Steenis CGGJ (1967) Miscellaneous botanical notes XVIII. Blumea 15:145–155Google Scholar
  36. Wheeler WM, Bequaert JC (1929) Amazonian myrmecophytes and their ants. Zool Anzeiger 82:10–39Google Scholar
  37. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols. Academic Press, London, pp 315–322Google Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2016

Authors and Affiliations

  • Shota Nakashima
    • 1
  • Emma Sarath
    • 2
  • Hiroshi Okada
    • 3
    • 4
  • Kazune Ezaki
    • 2
  • Dedy Darnaedi
    • 5
  • Hirokazu Tsukaya
    • 2
    • 6
  • Akiko Soejima
    • 1
  1. 1.Division of Biological Science, Graduate School of Science and TechnologyKumamoto UniversityKumamotoJapan
  2. 2.Graduate School of ScienceThe Univesity of TokyoTokyoJapan
  3. 3.Graduate School of ScienceOsaka City UniversityOsakaJapan
  4. 4.Institute of Natural Environmental SciencesHyogo Prefectural UniversitySandaJapan
  5. 5.Herbarium BogorienseResearch Center for Biology-LIPIBogorIndonesia
  6. 6.Bio-Next Project, Okazaki Institute for Integrative BioscienceNational Institutes of Natural SciencesOkazakiJapan

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