Friend or foe? A behavioral and stable isotopic investigation of an ant–plant symbiosis

Abstract

In ant-plant symbioses, the behavior of ant inhabitants affects the nature of the interaction, ranging from mutualism to parasitism. Mutualistic species confer a benefit to the plant, while parasites reap the benefits of the interaction without reciprocating, potentially resulting in a negative impact on the host plant. Using the ant-plant symbiosis between Cordia alliodora and its ant inhabitants as a model system, I examine the costs and benefits of habitation by the four most common ant inhabitants at La Selva Biological Station, Costa Rica. Costs are measured by counting coccoids associated with each ant species. Benefits include patrolling behavior, effectiveness at locating resources, and recruitment response. I also compare the diets of the four ant species using stable isotope analysis of nitrogen (N) and carbon (C). Ants varied in their rates of association with coccoids, performance of beneficial behaviors, and diet. These differences in cost, benefit, and diet among the ant species suggest differences in the nature of the symbiotic relationship between C. alliodora and its ants. Two of the ant species behave in a mutualistic manner, while the other two ant species appear to be parasites of the mutualism. I determined that the mutualistic ants feed at a higher trophic level than the parasitic ants. Behavioral and dietary evidence indicate the protective role of the mutualists, and suggest that the parasitic ants do not protect the plant by consuming herbivores.

The Direct and Ecological Costs of an Ant-Plant Symbiosis

“…Some phytoecious ants may consume nothing but extrafloral nectar and/or food bodies (e.g., Pheidole bicornis [Fischer et al 2002] and Pseudomyrmex on Acacia [Heil et al 2004]), even though they have been shown to significantly reduce herbivory on their hosts (Janzen 1967;Letourneau et al 1998), in which case they may reap only the indirect benefits of plant defense. But many, such as A. octoarticulatus, eat at least some of the insects that visit their host plants (e.g., Yu and Pierce 1998;Tillberg 2004). These ants are probably not under strong selection to cheat by not protecting their host plants against herbivores, and they might be expected to be more effective against palatable herbivores than unpalatable ones.…”

Indirect benefits of symbiotic coccoids for an ant-defended myrmecophytic tree

“…Colonies of A. pittieri usually have one queen and are limited to a single tree (E. G. Pringle, personal observation). A. pittieri ants patrol the leaves and stems of C. alliodora and attack herbivores and other intruders, biting and chasing them off the tree (Tillberg 2004; E. G. Pringle, R. Dirzo, and D. M. Gordon, personal observations). Reports differ on whether Azteca ants significantly reduce herbivory on C. alliodora leaves (Wheeler 1942, Tillberg 2004.…”

“…pittieri ants host both Coccidae (soft scale insects) and Pseudococcidae (mealybugs) inside domatia (Tillberg 2004) and eat their honeydew (E. G. Pringle, personal observation). Individual trees are usually inhabited by several species of coccids, including Cryptostigma reticulolaminae (both sites), Cryptostigma inquilina and Aztecalecanium sp.…”

“…Leaves grow in whorls near growing shoots where new domatia are produced. C. alliodora offers no plant-produced food rewards for ants, and Azteca ants always host coccoids inside the domatia where the ants nest (Wheeler 1942, Tillberg 2004; E. G. Pringle, personal observation). As early as 1902, the naturalist C. H. Tyler Townsend wrote to the entomologist W. M. Wheeler that the C. alliodora system constituted ''a most striking instance of the interrelations and mutual dependence of plant, ant, and coccid'' (Wheeler 1942:15-16).…”

Measuring the trophic ecology of ants using stable isotopes

“…army ants, Hirosawa et al, 2000), and a preponderance of omnivores (Blüthgen et al, 2003;Davidson et al, 2003). Recently, studies have utilized stable isotopes to elucidate the trophic ecology of ants including temporal variation in diet (Fisher et al, 1990;Mooney and Tillberg, in press), the nature of ant-plant symbioses (Treseder et al, 1995;Sagers et al, 2000;Solano and Dejean, 2004;Tillberg, 2004;Trimble and Sagers, 2004), and the community ecology of ants (Blüthgen et al, 2003;Davidson et al, 2003;Tillberg and Breed, 2004).…”