The Ants Chapter 14

CHAPTER 14. SYMBIOSES BETWEEN ANTS AND PLANTS

Odoardo Beccari, in his pioneering monograph on myrmecophilous plants (1884), reported that the East Indian pitcher plant Nepenthes bicalcarata harbors ant colonies in the hollow stem of the same pitcher-shaped leaf by which it captures and digests other kinds of insects (Figure 14-1). The ants are free to roam over the carnivorous plant and adjacent terrain, gathering insects and other food items of their own. If this relationship is verified, the ants and the plant appear to be engaged in a trade-off of mutual benefit (Jolivet, 1986). The ants risk being eaten by the plant but they get a home; the plants surrender some tissue space and insect prey to the ants but they gain some protection from herbivores.

The Nepenthe] story is only one, admittedly very peculiar case among hundreds of ant-plant symbioses documented during the past 150 years of research. This topic has been the subject of rich and informative reviews during the past ten years, including systematic accounts of the plants (Huxley, 1980, 1982; Jolivet, 1986), an ecological analysis of the proven cases of ant-plant mutualism (Beattie, 1985; Benson, 1985; Huxley, 1986), and a brief summary of all aspects of the symbioses with a bibliography complete through 1981 (Buckley, 1982a-c).

The varieties of ant-plant symbioses
The angiosperms (flowering plants) and the ants have been closely associated throughout most of their respective histories. By the middle of the Cretaceous Period primitive sphecomyrmine ants were on the scene, while the angiosperms were diversifying and spreading around the world as the newly dominant form of terrestrial vegetation. An intricate coevolution of the two groups probably began during this time. Many of the plant species had come to depend on insects for pollination, and an even greater number of insect species subsisted on nectar and pollen obtained during the pollination process. A legion of other insects fed on the foliage and wood of the angiosperms. Plants responded in turn by evolving various combinations of thick cuticles, dense spines and hairs, and secondary defense substances such as alkaloids and terpenes.

Into this lively theater of coevolution the ants entered. As the Cretaceous drew to a close, the ants increased in diversity and abundance, seized new roles as pollinators and seed dispensers, and appropriated the plants as domiciles. An entomologist returning to early Eocene times, about 60 million years ago, would find familiar-looking ants swarming over familiar-looking vegetation.

Complex symbioses have been fashioned among the thousands of species of ants and plants. Often these relationships are parasitic, with one exploiting the other and giving nothing in return. In other cases they are commensalistic, with one partner making use of the other but, as in the case of ants occupying hollow stems, neither harming nor helping it. But of maximum scientific interest, some symbioses appear to be mutualistic; in other words, both partners benefit from the association. To put the matter as briefly as possible, ants use cavities supplied by the plants for nest sites, as well as nectar and nutritive corpuscles given them as food. They in turn protect their plant hosts from herbivores, distribute their seeds, and literally pot their roots with soil and nutrients. There is abundant evidence, which we will review shortly, that some pairwise combinations of ants and plants have coevolved so that each is specialized to use the other's services. This mutualistic linkage has produced some of the most elaborate adaptations known in nature.

Before taking up these several categories and the evidence they provide for coevolution, let us define the specialized terms that have grown out of the study of ant-plant mutualism. The definitions below represent the concensus that we believe can be drawn from current usages.