Giant hogweed (Heracleum mantegazzianum), a weed originating from the Caucasus and invasive in Western Europe, is frequently observed with myrmecophilic aphids, ants, and non-myrmecophilic aphids. The number of individuals of the two non-myrmecophilic, leaf-sucking aphid species, Paramyzus heraclei and Cavariella theobaldi, are negatively correlated with the growth of giant hogweed in its native habitat. A cavity at the stem basis of giant hogweed, the domatium, lodges colonies of the obligate myrmecophilic, stem-sucking aphid Anuraphis subterranea. We found a positive correlation between relative plant growth, ant activity, and the number of myrmecophilic aphids. Because of the domatium size, A. subterranea populations are limited in growth and consequently the damage they inflict is limited. In contrast to the few other systems where three-partner mutualistic relationships are described, these partners appear to be more adapted to each other. This is the first report of an ant domatium from the temperate zone, and it is moreover the first experimental result presenting a system, from which a secondary domatium is able to evolve, because it is involving initial relations with aphids.
Agrawal, A.A., Karban, R. and R.G. Colfer. 2000. How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos 89: 70–80.
Aron, S., Beckers, R., Deneubourg, J.L. and J.M. Pasteels. 1993. Memory and chemical communication in the orientation of two mass-recruiting ant species. Insectes Soc. 40: 369–380.
Bach, C.E. 1991. Direct and indirect interactions between ants (Pheidole megacephala), scales (Coccus viridis) and plants (Pluchea indica). Oecologia 87: 233–239.
Baylis, M. and N. E. Pierce. 1991. The effect of host plant quality on the survival of larvae and oviposition behaviour of adults of an ant-tended lycaenid butterfly, Jalmenus evagoras. Ecol. Entomol. 16: 1–9.
Benson, W.W. 1985. Amazon ant-plants. In: Prance, G. T. and Lovejoy, T. E. (eds.), Key Environments. Amazonia. Pergamon Press. Oxford. pp. 239–266.
Bronstein, J. L. and P. Barbosa. 2002. Multitrophic/multispecies mutualistic interactions: the role of non-mutualists in shaping and mediating mutualisms. In: Hawkins, B. and T. Tscharntke (eds.), Multitrophic Level Interactions. Cambridge University Press, Cambridge. pp 44–65.
Buckley, R. 1983. Interaction between ants and membracid bugs decreases growth and seed set of host plant bearing extrafloral nectaries. Oecologia 58: 132–136.
Buckley, R.C. 1987. Interactions involving plants, Homoptera, and ants. Annu. Rev. Ecol. Syst. 18: 111–135.
Caroll, C. R. and D.H. Janzen. 1973. Ecology of foraging by ants. Annu. Rev. Ecol. Syst. 4: 231–257.
Dauber, J. and V. Wolters. 2000. Microbial activity and functional diversity in the mounds of three different ant species. Soil Biol. Biochem. 32: 93–99.
Davidson, D. W. and D. McKey. 1993. The evolutionary ecology of symbiotic ant – plant relationships. J. Hymenoptera. Research 2: 13–83.
El-Ziady, S. and J.S. Kennedy. 1956. Beneficial effects of the common garden ant, Lasius niger L., on the black bean aphid Aphis fabae Scopoli. Proc. R. Entomol. Soc. Lond. (A) 31: 61–65.
Fiala, B. and U. Maschwitz. 1992. Domatia as most important adaptations in the evolution of myrmecophytes in the paleotropical tree genus Macaranga (Euphorbiaceae). Plant Syst. Evol. 180: 53–64.
Grostal, P. and D.J. O’Dowd. 1994. Plants, mites and mutualism: leaf domatia and the abundance and reproduction of mites on Viburnum tinus (Caprifoliaceae). Oecologia 97: 308–315.
Gullan, P.J. 1997. Relationship with ants. In: Ben-Dov, Y. and Hodgson, C. J. (eds.), Soft scale insects, their biology - natural enemies and control. Elsevier Science, Amsterdam. pp 351–373.
Hansen, S.O. 2005. Interactions between the invasive weed Heracleum mantegazzianum and associated insects. PhD. thesis, University of Bern, Switzerland.
Hansen, S.O., Hattendorf, J., Wittenberg, R., Reznik, S.Y., Nielsen, C., Ravn, H.P. and W. Nentwig. 2006. Phytophagous insect fauna of the Giant Hogweed Heracleum mantegazzianum in invaded areas of Europe and in its native area of the Caucasus. Eur. J. Entomol. 103: 387–395.
Heie, O.E. 1992. The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. IV. Family Aphididae: Part 1 of tribe Macrosiphini of subfamily Aphidinae. Fauna Entomologica Scandinavica, Vol. 25, E.J.Brill/Scandinavian Science Press Ltd., Leiden.
Heil, M. and D, McKey. 2003. Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu. Rev. Ecol. Syst. 34: 425–553.
Hölldobler, B. and E.O. Wilson. 1990. The Ants. Harvard University Press, Cambridge. Mass.
Horstmann, K. 1974. Investigations on food-consumption of red wood ants (Formica polyctena Foerster) in an oak forest. 3. Annual turnover. Oecologia 15: 187–204.
Horstmann, K. 1982. The energy budget of wood ants (Formica polyctena Forster) in an oak forest. Insectes Soc. 29: 402–421.
Howell, J.F. and P.A. Games. 1974. The effects of variance heterogeneity on simultaneous multiple-comparison procedures with equal sample size. Brit. J. Math. Stat. Psychol. 27: 72–81.
Itino, T., Itioka, T., Hatada, A. and A.A. Hamid. 2001. Effects of food rewards offered by ant-plant Macaranga on the colony size of ants. Ecol. Res. 16: 775–786.
Janzen, D.H. 1979. How to be a fig. Annu. Rev. Ecol. Syst. 10: 13–51.
Jolivet, P. 1996. Ants and Plants. An Example of Coevolution. Backhuys publishers, Leiden.
Koptur, S. 1984. Experimental evidence for defense of Inga (Mimosoideae) saplings by ants. Ecology 65: 1787–1793
Messina, F.J. 1981. Plant protection as a consequence of an antmembracid mutualism: interactions on goldenrod (Solidago sp.). Ecology 62: 1433–1440.
Morales, M.A. 2000. Mechanisms and density dependence of benefit in an ant-membracid mutualism. Ecology 81: 482–489.
Nakamura, T., Taniguchi, T. and E. Maeda. 1992. Leaf anatomy of Coffea arabica L. with reference to domatia. Jap. J. Crop Sci. 61: 642–650.
O’Dowd, D. J. and E.A. Catchpole. 1983. Ants and extrafloral nectaries: no evidence for plant protection in Helichrysum spp.–ant interactions. Oecologia 59: 191–200.
Offenberg, J. 2000. Correlated evolution of the association between aphids and ants and the association between aphids and plants with extrafloral nectaries. Oikos 91: 146–152.
Offenberg, J. 2001. Balancing between mutualism and exploitation: the symbiotic interaction between Lasius ants and aphids. Behav. Ecol. Sociobiol. 49: 304–310.
Offenberg, J., Nielsen, M.G., MacIntosh, D.J., Havanon, S. and S. Aksornkoae. 2004. Evidence that insect herbivores are deterred by ant pheromones. Proc. R. Soc. Lond. (B) 271: 433–435.
Pysek, P. and A. Pysek. 1995. Invasion by Heracleum mantegazzianum in different habitats in the Czech Republic. J. Veg. Sci. 6: 711–718.
Schnell, R., Cusset, G., Tchinaye, V. and N.T. Anh. 1968. Contribution à l’étude des “acarodomaties”. La question des aisselles des nervures. Rev. Gén. Bot. 75: 5–64.
Skinner, G.J. 1980 The feeding habits of the wood-ant, Formica rufa (Hymenoptera: Formicidae), in limestone woodland in Northwest England. J. Anim. Ecol. 49: 417–433.
Stadler, B. and A.F.G. Dixon. 2005. Ecology and evolution of aphidant interactions. Annu. Rev. Ecol. Evol. Syst. 36: 345–372.
Thompson, J.N. 1994. Coevolutionary Process. The University of Chicago Press, Chicago.
Vasconcelos, H.L. 1993. Ant colonization of Maieta guianensis seedlings, an Amazon ant-plant. Oecologia 95: 439–443.
Vrieling, K., Smit, W. and E. van der Meijden. 1991. Tritrophic interactions between aphids (Aphis jacobaeae Schrank), ant species, Tyria jacobaeae L., and Senecio jacobaea L. lead to maintenance of genetic variation in pyrrolizidine alkaloid concentration. Oecologia 86: 177–182.
Way, M.J. 1954. Studies on the association of the ant Oecophylla longinoda (Latr.) (Formicidae) with the scale insect Saissetia zanzibarensis Willams (Coccidae). B. Entomol. Res. 45: 113–134.
Way, M.J. 1963. Mutualism between ants and honey dew producing Homoptera. Annu. Rev. Entomol. 8: 307–344.
Weber, H. 1968. Biologie der Hemipteren. A. Asher & Co., Amsterdam. pp 460–508.
Zar, J.H. 1996. Biostatistical analysis. Prentice Hall, London.
About this article
Cite this article
Hansen, S.O., Hattendorf, J. & Nentwig, W. Mutualistic relationship beneficial for aphids and ants on giant hogweed (Heracleum mantegazzianum). COMMUNITY ECOLOGY 7, 43–52 (2006). https://doi.org/10.1556/ComEc.7.2006.1.5
- Anuraphis subterranea
- Invasive weed