Journal of Plant Research

, Volume 132, Issue 4, pp 499–507 | Cite as

Extrafloral nectary-bearing plant Mallotus japonicus uses different types of extrafloral nectaries to establish effective defense by ants

  • Akira YamawoEmail author
  • Nobuhiko Suzuki
  • Jun Tagawa
Regular Paper


Extrafloral nectary (EFN)-bearing plants attract ants to gain protection against herbivores. Some EFN-bearing plants possess different types of EFNs, which might have different effects on ants on the plants. Mallotus japonicus (Thunb.) Muell. Arg. (Euphorbiaceae) bears two types of EFNs, including a pair of large EFNs at the leaf base and many small EFNs along the leaf edge. This study aimed to determine the different roles of the two types of EFNs in biotic defense by ants. A field experiment was conducted to investigate the effect of leaf damage on EFN production and on the distribution pattern of ants. After leaf damage, the number of leaf edge EFNs increased in the leaves first-produced. The number of ants on the leaves also increased, and the foraging area of ants extended from the leaf base to the leaf tip. An EFN-covering field experiment revealed that leaf edge EFNs had a greater effect than leaf base EFNs on ant dispersal on leaves. The extended foraging area of ants resulted in an increase of encounter or attack rate against an experimentally placed herbivore, Spodoptera litura. These results suggest that M. japonicus plants control the foraging area of ants on their leaves using different types of EFNs in response to leaf damage, thus achieving a very effective biotic defense against herbivores by ants.


Ant–plant mutualism Biotic defense EFN Induced defense Leaf damage 



We thank N. Katayama and K. Tanaka for useful comments on the manuscript. This work was supported in part by a research fellowship from the Japan Society for the Promotion of Science for Young Scientists (234305 and 251712).

Supplementary material

10265_2019_1119_MOESM1_ESM.pdf (140 kb)
Supplementary material 1 (PDF 139 kb)


  1. Armbruster WS (1993) Evolution of plant pollination systems: hypotheses and tests with the neotropical vine Dalechampia. Evolution 47:1480–1505CrossRefGoogle Scholar
  2. Baker HG, Opler PA, Baker I (1978) A comparison of the amino acid complements of floral and extrafloral nectars. Bot Gaz 139:322–332CrossRefGoogle Scholar
  3. Bixenmann RJ, Coley PD, Kursar TA (2011) Is extrafloral nectar production induced by herbivores or ants in a tropical facultative ant-plant mutualism? Oecologia 165:417–425CrossRefGoogle Scholar
  4. Bronstein JL (1998) The contribution of ant–plant protection studies to our understanding of mutualism. Biotropica 30:150–161CrossRefGoogle Scholar
  5. Bull JJ, Rice WR (1991) Distinguishing mechanisms for the evolution of co-operation. J Theor Biol 149:63–74CrossRefGoogle Scholar
  6. de la Fuente MAS, Marquis RJ (1999) The role of ant-tended extrafloral nectaries in the protection and benefit of a Neotropical rainforest tree. Oecologia 118:192–202CrossRefGoogle Scholar
  7. Delgado MN, Somavilla NS, Báo SN, Rossatto DR (2017) Testing the optimal defense hypothesis in Stryphnodendron adstringens (Fabaceae, Mimosoideae) leaves: the role of structure, number, position and nectar composition of extrafloral nectaries. Plant Spec Biol 32:333–339CrossRefGoogle Scholar
  8. Development R (2012) R: a language and environment for statistical computing. Austria, ViennaGoogle Scholar
  9. Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Nat Acad Sci USA 95:8676–8680CrossRefGoogle Scholar
  10. Escalante-Pérez M, Jaborsky M, Lautner S, Fromm J, Müller T, Dittrich M, Kunert M, Boland W, Hedrich R, Ache P (2012) Poplar extrafloral nectaries: two types, two strategies of indirect defenses against herbivores. Plant Physiol 159:1176–1191CrossRefGoogle Scholar
  11. Fahn A (1987) The extrafloral nectaries of Sambucus nigra. Ann Bot 60:299–308CrossRefGoogle Scholar
  12. Ferriere R, Bronstein JL, Rinaldi S, Law R, Gauduchon M (2002) Cheating and the evolutionary stability of mutualisms. Proc R Soc Lond B 269:773–780CrossRefGoogle Scholar
  13. Grasso DA, Pandolfi C, Bazihizina N, Nocentini D, Nepi M, Mncuso S (2015) Extrafloral-nectar-based partner manipulation in plant-ant relationships. AoB Plants 7:plv002CrossRefGoogle Scholar
  14. Heil M (2013) Let the best one stay: screening of ant defenders by Acacia host plants functions independently of partner choice or host sanctions. J Ecol 101:684–688CrossRefGoogle Scholar
  15. Heil M, Barajas-Barron A, Orona-Tamayo D, Wielsch N, Svatos A (2014) Partner manipulation stabilises a horizontally transmitted mutualism. Ecol Lett 17:185–192CrossRefGoogle Scholar
  16. Koptur S (1992) Extrafloral nectary-mediated interactions between insects and plants. In: Bernays EA (ed) Insect–plant interactions, vol 4. CRC Press, Boca Raton, pp 81–129Google Scholar
  17. Kowarik I, Säumel I (2007) Biological flora of Central Europe: Ailanthus altissima (Mill.) Swingle. Perspect Plant Ecol 8:207–237CrossRefGoogle Scholar
  18. Leigh EG Jr (2010) The evolution of mutualism. J Evol Biol 23:2507–2528CrossRefGoogle Scholar
  19. Millán-Cañongo C, Orona-Tamayo D, Heil M (2014) Phloem sugar flux and jasmonic acid-responsive cell wall invertase control extrafloral nectar secretion in Ricinus communis. J Chem Ecol 40:760–769CrossRefGoogle Scholar
  20. Ness JH (2003) Catalpa bignonioides alters extrafloral nectar production after herbivory and attracts ant bodyguards. Oecologia 134:210–218CrossRefGoogle Scholar
  21. O’Dowd DJ (1979) Foliar nectar production and ant activity on a neotropical tree, Ochroma pyramidale. Oecologia 43:233–248CrossRefGoogle Scholar
  22. Offenberg J, Nielsen MG, Maclntosh DJ, Havanon S, Aksornkoae S (2004) Evidence that insect herbivores are deterred by ant pheromones. Proc R Soc Lond B 271:433–435CrossRefGoogle Scholar
  23. Pulice CE, Packer AA (2008) Simulated herbivory induces extrafloral nectary production in Prunus avium. Funct Ecol 22:801–807CrossRefGoogle Scholar
  24. Radhika V, Kost C, Bartram S, Heil M, Boland W (2008) Testing the optimal defence hypothesis for two indirect defences: extrafloral nectar and volatile organic compounds. Planta 228:449–457CrossRefGoogle Scholar
  25. Rios RS, Marquis RJ, Flunker JC (2008) Population variation in plant traits associated with ant attraction and herbivory in Chamaecrista fasciculata (Fabaceae). Oecologia 156:577–588CrossRefGoogle Scholar
  26. Sakata H, Katayama N (2001) Ant defence system: a mechanism organizing individual responses into efficient collective behavior. Ecol Res 16:395–403CrossRefGoogle Scholar
  27. Suzuki MF, Ohashi K (2014) How does a floral colour-changing species differ from its non-colour changing congener?—a comparison of trait combinations and their effects on pollination. Funct Ecol 28:549–560CrossRefGoogle Scholar
  28. Tilman D (1978) Cherries, ants and tent caterpillars: timing of nectar production in relation to susceptibility of caterpillars to ant predation. Ecology 59:686–692CrossRefGoogle Scholar
  29. Vander Wall SB (2010) How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philos Trans R Soc Lond B 365:989–997CrossRefGoogle Scholar
  30. Washitani I, Takenaka A (1987) Gap-detecting mechanism in the seed germination of Mallotus japonicus (Thunb.) Muell. Arg., a common pioneer tree of secondary succession in temperate Japan. Ecol Res 2:191–201CrossRefGoogle Scholar
  31. Wilder SM, Eubanks MD (2010) Extrafloral nectar content alters foraging preferences of a predatory ant. Biol Lett 6:177–179CrossRefGoogle Scholar
  32. Wooley SC, Donaldson JR, Gusse AC, Lindroth RL, Stevens MT (2007) Extrafloral nectaries in aspen (Populus tremuloides): heritable genetic variation and herbivore-induced expression. Ann Bot 100:1337–1346CrossRefGoogle Scholar
  33. Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA, Power EF, Borland AM, Stevenson PC (2013) Caffeine in floral nectar enhances a pollinator’s memory of reward. Science 339:1202–1204CrossRefGoogle Scholar
  34. Yamawo A, Suzuki N (2018) Induction and relaxation of extrafloral nectaries in response to simulated herbivory in young Mallotus japonicus plants. J Plant Res 131:255–260CrossRefGoogle Scholar
  35. Yamawo A, Katayama N, Suzuki N, Hada Y (2012a) Plasticity in the expression of direct and indirect defence traits of young plants of Mallotus japonicus in relation to soil nutritional conditions. Plant Ecol 213:127–132CrossRefGoogle Scholar
  36. Yamawo A, Suzuki N, Tagawa J, Hada Y (2012b) Leaf ageing promotes the shift in defence tactics in Mallotus japonicus from direct to indirect defence. J Ecol 100:802–809CrossRefGoogle Scholar
  37. Yamawo A, Tagawa J, Hada Y, Suzuki N (2014) Different combinations of multiple defence traits in an extrafloral nectary-bearing plant growing under various habitat conditions. J Ecol 102:238–247CrossRefGoogle Scholar
  38. Yamawo A, Tokuda M, Katayama N, Yahara T, Tagawa J (2015) Ant-attendance in extrafloral nectar-bearing plants promotes growth and decreases the expression of traits related to direct defenses. Evol Biol 42:191–198CrossRefGoogle Scholar
  39. Yamawo A, Hada Y, Tagawa J (2017) Aggressiveness of ants attracted to the extrafloral nectary-bearing plant, Mallotus japonicus, and temporal fluctuations in their abundance. Entomol Sci 20:150–155CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Applied Biological Sciences, Faculty of AgricultureSaga UniversitySagaJapan
  2. 2.Department of Biosphere–Geosphere System Science, Faculty of InformaticsOkayama University of ScienceOkayamaJapan

Personalised recommendations