Allelopathy by Myrmecophytes: The Ant Azteca as an Allelopathic Agent of Cecropia

Azteca ants, that obligatorily live in neotropical second-growth trees of the genus Cecropia, kill vine ends that begin to climb on the Cecropia trunk. Presumably this aids the Cecropia tree in its efforts to maintain an emergent position in the general canopy, and may be one of the selective advantages of being occupied by an Azteca colony. This system is, in both process and pattern, extremely similar to that of the swollen-thorn acacias and their ant occupants. In both cases the ants are effectively allelopathic agents, and are functionally analogous to the chemicals liberated by some plants in their competitive interactions with other plants; like these chemicals, the ants are "produced" at a metabolic cost to the plant. The ants may, however, be a more efficient allelopathic agent than a chemical because of their versatility. Since the original descriptions of the apparently mutualistic association between lowland second-growth trees in the neotropical genus Cecropia (Moraceae) and the Azteca ants that obligatorily occupy them (Muller 1874, 1880, Belt 1874), there has been a running argument as to whether the ants are in any sense "needed" by the plant (Bequaert 1922, Wheeler 1942, Ihering 1907, Eidmann 1944, Bailey 1922, Brown 1960, etc.). That the argument survives is due to two apparently opposing sets of observations. Favoring a mutualistic interpretation, the known species of Cecropia have several apparent adaptations to the ants: (1) exceptionally large hollow internodes in which the ants live and tend Homoptera that produce honeydew (exceptions appear secondarily derived and are discussed below), (2) regularly occurring thin spots in the internode wall where the worker and founding queen ants gain entrance to the internode, and (3) "Mullerian bodies" (lipid, protein and carbo1 Contribution No. 1396 of the Department of Entomology, University of Kansas, Lawrence, Kansas. This study was supported by NSF Grant No. GB-5206 and the teaching program, of the Organization for Tropical Studies. 2 Present address: Department of Biology, University of Chicago, Chicago 60637. hydrate-rich food bodies) continually growing from highly modified petiole bases (these tiny bodies are apparently the primary food source of the colony and are harvested and fed to the larvae). While not all species of the primarily arboreal, neotropical ant genus A.teca are involved in this system, at least 10 species are in an apparently obligate manner (Wheeler 1942, and see also for a general discussion of the biology of Ateca). The functional significance of the first two of the three genetically determined morphological traits of Cecropia listed above has been inadequately "explained" in terms of structural strengthening (Ihering 1907, Bailey 1922) and as an accidental by-product of usual developmental processes (Bailey 1922), respectively. The third trait cannot be explained in this manner. Unless the ant colony's presence is considered to be of positive selective value to the tree, there is no obvious selective basis for the presence of these three traits. However, the only immediately obvious aggression by the ants is against humans that are cutting Cecropia trees, despite numerous postulations that the ants should protect the tree from a large variety of herbivores, including leaf-cutter ants. Further, it is commonplace to encounter occupied Cecropia with foliage heavily eaten by insects, and healthy unoccupied Cecropia are apparently not rare This content downloaded from 157.55. 39.17 on Fri, 02 Sep 2016 04:34:29 UTC All use subject to http://about.jstor. org/terms 148 REPORTS Ecology, Vol. 50, No. 1 in some habitats. The obvious field experiments needed to clarify the situation had not been attempted. This apparently contradictory situation, accompanied by similar arguments, was the state of the art for all apparent mutualistic associations between plants with ants living in them (myrmecophytes), until it was experimentally demonstrated that two Central American swollen-thorn acacias (Acacia cornigera and A. collinsii; Leguminosae) are obligatorily dependent in nature upon their ant occupants (Pseudomnyrmex spp.; Pseudomyrmecinae) for survival to reproductive maturity (Janzen 1967a and unpublished). Further, the ant-acacia myrmecophytic relationship is a very highly coevolved one (Janzen 1966) and applies to all 10 of the normally occupied swollen-thorn acacia species in Central America. The demonstration of mutualism between Pscudo11nyrwnex and Acacia throws a new light on the Cecropia and Asteca interaction, especially since the general extent of herbivore damage to swollen-thorn acacias is very similar to that of Cecropia. Further, the only immediately obvious aggression demonstrated by Pseudomyrinex is against large vertebrates, and like Cecropia, apparently healthy but unoccupied swollen-thorn acacias are occasionally encountered in nature. However, detailed analysis has shown that Pseudoinyrnmex workers remove most phytophagous insects and kill the intrusive branches of vines and shrubs in the acacia canopy. If the ants are experimentally removed, the combination of greatly increased insect damage and shading from adjacent plants in the rapidly growing adjacent second growth -severely stunts the plant and eventually results in death. Further, a partial "fire-break" may on occasion result from the ants' pruning activities (Janzen 1967b). Alone, either browsing by insects or shading will kill the acacia, but they are faster and more effective when operating together. The analogous experiments with Cecropia (and two other myrmecophytes, Cordia and Triplaris) are presently in progress in Costa Rica, but I would like to draw attention at this time to one activity of worker Axteca ants that very likely influences the survival and general health of the Cecropia they occupy. By chewing on them, worker A teca kill the shoot tips _ f . = . S.C::,',. Aj~~~~~~~~~~~~~~f,:. ',. , i . A. ,. A. A. i r. '. ,. p w. ; . I ; ,. I FIG. 1. On the right are two vine ends of a convolvulaceous vine that have been chewed off and killed by Azteca worker ants where the vine touched the Cecropia. The vine on the right has also had one leaf completely pruned off and the other severely trimmed. The two vines on the left and extending up over the top of the photograph are intact examples from the same plant (8 March 1968; Osa Peninsula, Costa Rica). and tendrils of vines that attempt to climb Cecropia trunks or enter the canopy laterally (Fig. 1); they in effect make the occupied Cecropia tree capable of allelopathy. Studies of allelopathy (as defined by Molisch 1937) have focused on chemical inhibition of neighboring plants (Muller, Muller, and Baines 1964, Muller 1966, Borner 1960, Woods 1960) and the mechanics of the process. However, the phenomenon may be generalized as a competitive process (of an interference type), or model, whereby one organism is responsible for the input into the environment of an object that is inimical to the development of a competitor (i.e., competitive interference where the adaptive value is in the elimination of a competitor). Here, the severe destruction of vegetation around swollen-thorn acacias by obligate acacia ants (Janzen 1967a) is clearly analogous to the inhibition of herbaceous growth around the shrubs Arteniesia and Salvia by volatile compounds (Muller et al. 1964, Muller 1966) and other classical cases of allelopathy. As is likely the case with the chemicals active in allelopathy, the ants are "produced" by the plant in a very real sense, in respect to the cost of maintaining them and the selection for traits promoting their presence. Barnwell (1967), while discussing activity patterns, first described damage to other plants by Azteca cf. alfari on Cecropia obtusifolia (near Puerto Viejo, Heredia Prov., Costa Rica): "the ants . were cutting deeply into the stem and leaves of a cucurbit . where it had contacted the Cecropia. Similarly, at the C. peltata in Guanacaste the leaves of an adjacent shrub had been neatly cut back from the lower trunk of the tree. " He then postulated that "there is the possibility that the cutting back of overgrowth contributes to the survival and reproduction of Cecropia . " I would like to support this hypothesis as a special case of allelopathic interference competition, and discuss its relationship to the hitherto unsatisfactorily explained aggression to plants shown by several genera of ants occupying myrmecophytes other than Cecropia and Acacia.