In his massive elegy, “In Memorium A. H. H.”, Alfred, Lord Tennyson laments the death of his friend, Arthur Henry Hallam, at 22 years old. Tennyson writes,
“Who trusted God was love indeed
And love Creation’s final law
Tho’ Nature, red in tooth and claw
With ravine, shriek’d against his creed”
Thus Tennyson accuses the natural world of being rife with strife and violence.
It would be wrong to dispute Tennyson’s complaint outright, but ecologists can present mutualisms, interactions in which both species benefit, as a counterpoint to his argument. One of the best studied is the ant/acacia tree mutualism, in which acacia trees provide food and living accommodations to ants, which protect their home tree against herbivores, including immense creatures such as elephants and giraffes! Previous research had shown that acacias usually grew better if they harbored a colony of protective ants, even though they were providing the ants with costly resources. These resources included swollen thorns (domatia) which ants may use as homes or fungal gardens, and specialized structures (nectaries) which provide ants with sugar.
As an undergraduate at the University of Florida, Patrick Mulligan learned about how ecology could be thought of as the study of the economy of nature. Keeping with the economic metaphor, Mulligan recognized that the tiny ants and relatively large trees trade in the same currency: carbon. He realized that tree growth is simply a measure of how much carbon a tree has to spend on itself. So he asked if ants might be influencing how much carbon is available for both themselves and the tree.
In Laikipia, Kenya, four ant species compete for Acacia drepanolobium host plants, the dominant woody plant in the savanna (see photo above). These ants differ in several traits including how much protection they actually provide, whether they consume tree-produced nectar, how they modify the tree, and how they influence a tree’s water relations (see photo and table below). If a tree can’t get enough water, it is forced to close the stomata on its leaf surface to reduce water loss from transpiration. When stomata are closed, carbon dioxide import is drastically curtailed, and photosynthetic rates (and carbon production) are reduced.
To determine how the four ant species influence carbon fixation and water relations in these acacias, Milligan and his colleagues set up a five-year ant-removal experiment between 2013-2018. They found 48 matched pairs of trees that harbored each ant species (12 pairs of trees per ant species), and then removed all of the ants from one of the two trees by fogging with a short-lived insecticide. The researchers restricted ant recolonization by applying to the base of each tree an annoyingly sticky substance that ants generally avoid.
After five years (in 2018), Milligan and his colleagues measured photosynthesis and transpiration rates in leaves of each tree, using tools that were specialized for those purposes. They then extrapolated from these leaf measurements to photosynthetic and water exchange rates for the entire tree crown (where most of the action is). They discovered that trees with C. mimosae (Cm) and T. penzigi (Tp) had substantially higher photosynthetic rates than trees with C. sjostedti(Cs) and C. nigriceps (Cn). But trees that had their ants removed were statistically indistinguishable in their photosynthetic rates (graph (a) below). In other words, removing ants caused Cm and Tp-trees to reduce their photosynthetic rates, and Cs and Cn tree to increase their photosynthetic rates, so they were equivalent after five years of ant removal.
Looking at the table above, you will note that both Cs and Cn do some major alterations to the trees that might compromise carbon production. Though Tp does remove nectaries, it also consumes no nectar, so that interaction may be a wash. Based on these observations, we might suspect that Cs and Cn are actually tree parasites, while while Cm and Tp are closer to true mutualists that actually benefit the host trees. Supporting this idea, removing Cs sharply increased leaf area and also increased water exchange rate (graph (b) above). And trees that were continuously occupied by Cn also showed reduced leaf area, lower photosynthetic rates (graph a above) and water exchange rates (graph b above) at the tree crown than Cm or Tp. But there is more to the story.
Cn is an aggressive defender against would-be herbivores. However, it also eats large portions of the tree it inhabits focusing on the nectaries (which produce sugars) and the reproductive structures. One puzzling consequence of this behavior is that Cn-occupied trees are significantly better than other ant-occupied trees at bringing up subsurface water, perhaps helping the tree to survive droughts. The researchers plan to measure the root systems of all the trees in hopes of seeing whether Cn-occupation actually alters root development in a way that improves water uptake.
Complicating the story further is a consideration of carbohydrate production. Trees hosting Cs (the stem excavator) had much less starch in their stems than did trees hosting the other species. Starch is an important source of energy for all plants; in fact trees with Cs removed still had low starch levels after five years. Presumably the trees that were freed from hosting Cs prioritized growing new branches, or repairing cavities and defending against beetle infestation, over producing more starch for storage.
Trees occupied by Cm (a nectar consumer) had much higher glucose levels than trees hosting the other three species. Removing Cm caused the glucose levels to drop sharply (see graph below). Trees hosting the other nectar consumer (Cn) did not show this increase in glucose, possibly because Cn prunes the leaves and eats the flowers, leaving the host tree with insufficient nutrients to increase glucose levels.
I asked Patrick Milligan how trees get occupied by a particular ant species. He responded that there are battles for occupancy both between ant species, and sometimes within ant species. An ant from one colony locks in a death grip with an ant from another colony, they then fall from a branch and kill each other on the ground. So the bigger colony wins a battle by virtue of having some surviving ants to colonize the tree. One exception is Cs, which has slightly larger and presumably stronger ants, and will sometimes survive a head-to-head battle. Currently, Milligan and his colleagues are investigating how a tree may adjust its leaf physiology when paired with a new ant species, perhaps by activating different genes in response to the novel species. Though trees cannot choose their ant colonizers, they may be able to adjust to whichever species uses their services.
note: the paper that describes this research is from the journal Ecology. The reference is Milligan, P.D., Martin, T.A., Pringle, E.G., Prior, K.M. and Palmer, T.M., 2023. Symbiotic ant traits produce differential host‐plant carbon and water dynamics in a multi‐species mutualism. Ecology, 104(1), p.e3880. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2023 by the Ecological Society of America. All rights reserved.