Ants and acacias: friends, foes or frenemies?

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.

Swollen thorns (domatia) on an Acacia drepanolobium tree that is hosting Crematogaster nigriceps ants. Credit: Patrick Milligan.

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.

Acacia drepanolobium, the dominant tree in the savanna. Credit Patrick Milligan.

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.

The four ants species studied by Patrick Milligan and his colleagues are Crematogaster sjostedti, C, mimosae, C. nigriceps and Tetraponera penzigi. Credit: Todd Palmer.

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.  

(Graph a) Mean (+SE) photosynthetic rate at the tree crown and (Graph b) transpiration rate at the tree crown for acacia trees with ants present or removed. The letters to the side of each data point indicate when two species have statistically significant differences in their value. For example, in graph a, comparing the case where ants were present, the photosynthetic rates for Cm and Tp are not different from each other, but both are significantly greater than the photosynthetic rates for Cn and Cs. However, Cn and Cs have similar photosynthetic rates.

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. 

Mean (+SE) glucose levels in the stems of trees hosting each ant species. Notice the sharp drop in glucose concentration five years after Cm removal.

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. Ecology104(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.

Too much of a good thing is killing Monarch butterflies

There was a time in the mid-Pleisticine when a photo of an ecological event was an awesome novelty, and a movie of an ecological event even more so.  Dodderers of an ecological bent (myself included), can vividly recall viewing a series of photos or a movie, either in a seminar or in an ancient ecology text, of a blue jay consuming a monarch butterfly, Danaus plexippus.  Consumption is immediately followed by explosive vomiting, as the cardenolides within the monarch butterfly claim another victim.  The monarch sequesters these cardenolide toxins from its larval food (milkweed), and incorporates them into its tissues as a means of protecting itself from predators – presumably blue jays learn from this very aversive experience.  I should point out that the individual sacrificial butterfly enjoys no fitness from this learning event – which raises some evolutionary questions we will not explore at the present.

Karen Oberhauser

Five instars (stages of development) of monarch caterpillars on a milkweed leaf. Credit: Karen Oberhauser

Rather we turn our attention to the relationship between milkweed, monarchs, and climate change. In several places in this blog we’ve talked about how climate change has influenced the behavior or physiology of a single species. For example, my first blog (Jan 31, 2017) discusses how increasing temperatures create more females in a loggerhead turtle population. But there are fewer studies that explore how climate change influences the ecological landscape, ultimately affecting interactions between species.  Along these lines, Matt Faldyn wondered if increased air temperature would change the chemical constitution of milkweed in a way that might influence monarch populations.  As he describes, “With milkweed toxicity, there is a ‘goldilocks’ zone where monarchs prefer to feed on milkweed that produce enough toxins in order to sequester these (cardenolide) chemicals as an antipredator/antiparasite defense, while also avoiding reaching a tipping point of toxicity where feeding on very toxic milkweeds negatively impacts monarch fitness.” He expected that at higher temperatures, milkweed would become stressed, and be physiologically unable to sustain normal levels of cardenolide production.


Monarch butterfly feeds on a native milkweed, Asclepias incarnata. Credit: Teune at the English Language Wikipedia.

For their research, Faldyn and his colleagues worked with two milkweed species.  Asclepias incarnata is a common, native milkweed found throughout the monarch butterfly’s range in the eastern and southeastern United States.  Asclepias curassavica is an exotic species that has become established in the southern United States.  In contrast to A. incarnata, A. curassavica does not die back over the winter months; consequently some monarch populations are no longer migratory, relying on A. curassavicato provide them with a year round food supply.


The exotic milkweed, Asclepias curassavica. Credit: 2016 Jee & Rani Nature Photography (License: CC BY-SA 4.0)

To protect against herbivory, milkweeds have two primary chemical deterrants: (1) the already-mentioned cardenolides, which are toxic steroids that disrupt cell membrane function, and (2) release of sticky latex, which can gum up caterpillar mouthparts and actually trap young caterpillars.

field_noborderii.jpgThe researchers wanted to simulate climate change under field conditions, so they created open-top chambers with plexiglass plates that functioned much like mini-greenhouses, into which they placed one milkweed plant that was covered with butterfly netting.  This setup raised ambient temperatures by about 3°C during the day and 0.2°C at nighttime.  Control plots were single milkweed plants with butterfly netting. Half of the plants were native milkweed, and the other half were the exotic species.

For their experiments, Faldyn and his colleagues introduced 80 monarch caterpillars (one per plant) and allowed them to feed normally until they pupated.  Pupae were brought into the lab and allowed to metamorphose into adults.


Matt Faldyn holds two monarch butterflies in the laboratory. Credit Matt Faldyn.

At normal (ambient) temperatures, monarchs survived somewhat better on exotic milkweed.  But at warmer temperatures, there is a strikingly different picture. Monarch survival is unaffected by warmer temperatures on native milkweed, but is sharply reduced by warmer temperatures on exotic milkweed (top graph below). The few that managed to survive warm temperatures on exotic milkweed grew much smaller, based on their body mass and forewing length (middle and bottom graph below)


Survival (top), adult mass (middle) and forewing length (bottom) of monarch butterflies raised under normal (ambient) and warmed temperatures.  Error bars are 95% confidence intervals.

Both milkweed species increased production of both types of chemicals over the course of the experiment. But by the end of the experiment, the exotic species released 3-times the quantity of latex and 13-times the quantity of cardenolides than did the native milkweed species.


Average amount of latex released at the beginning and end of the experiment.  Error bars are 95% confidence intervals.


Average cardenolide concentration at the beginning and end of the experiment.

The researchers argue that the exotic milkweed, Asclepias curassavica, may become an ecological trap for monarch butterflies, in that it attracts monarchs to feed on it, but will, under future warmer conditions, result in dramatically reduced monarch survival. Interestingly, these results are not what Faldyn originally expected; recall that he anticipated that temperature-stressed plants would reduce cardenolide production. The tremendous increase in cardenolide production in exotic milkweed at warmer temperatures may simply be too much toxin for the monarchs to process. The researchers predict that as climate warms, milkweed ranges will expand further north into Canada, and lead to northward shifts of monarch populations as well.  They urge nurseries to emphasize the distribution of native rather than exotic milkweed, so that monarchs will be less likely to become victims of this ecological trap.

note: the paper that describes this research is from the journal Ecology. The reference is Faldyn, M. J., Hunter, M. D. and Elderd, B. D. (2018), Climate change and an invasive, tropical milkweed: an ecological trap for monarch butterflies. Ecology. doi:10.1002/ecy.2198. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.