an overview

Two impressive genera unite

Cecropia is one of the most prominent and unique genera of pioneer plants in the neotropics. With over 60 species ranging from southern Mexico to northern Argentina (1), the plant's unrivaled success is due to a number of specialized adaptations - most notably its intimate symbiosis with Azteca ants. Ants in the genus Azteca are notoriously aggressive and carnivorous, often dominating the forest canopy. At least 13 species are obligate symbionts of Cecropia trees (2). The unity of these two genera goes back 8 million years (3) to form one of the most impressive mutualisms in the world.

 

In the beginning

 

A newly mated queen
and a hospitable sapling . . .

This newly mated queen chews a hole at a designated site on a hollow internode of a half-meter Cecropia sapling. This site opposite the leaf petiole, called a prostomata, looks like a dimple where the plant's wall is shallow and designed for ant excavation (4). Once inside, she scrapes the internal tissue, called parenchyma, and uses it to plug the hole (5). She will lay eggs and tend to the larvae until the first workers emerge and reopen the hole.

The queen is often not alone, and
competition ensues

 

When a queen enters a Cecropia internode, she may not be the first one there. If she lands on a sapling in which workers have not emerged yet, the queen can enter an internode that is already occupied by queens. Commonly, two to five queens inhabit the same internode and cooperate in raising brood together. Thus, each internode functions as its own cohesive colony after the workers emerge. Every tree potentially contains several multi-queen colonies who compete for dominance over the tree, mostly by excluding other colonies from collecting the plant's food bodies. Patrolling workers also attack and kill new queens that land on the tree looking to start a colony (6)

Only one will prevail

After one colony reigns supreme and eliminates all other colonies, a period of ergonomic growth follows. Both the winning colony and the tree grow considerably in size over a few months of stockpiling food bodies. At this point, the cooperating queens turn on each other, likely concerned with the production of sexuals, new queens and males, that will fly off and pass their genes on. The queens gruesomely fight to the death, tearing limbs and severing segments, until one queen is victorious, remaining as the sole reproductive for the rest of the colony's life (6).

From a queen's perspective, multi-queen colonies are advantageous over single-queen colonies in the first stage of competition because they can quickly produce more workers that help them gain control of the tree. However, when the colony has the resources to produce new queens and males, the genes being passed on may be split between the remaining queens. Thus, it is advantageous to a queen to be the only reproductive, so she can ensure all offspring are hers (6).

 

Mutualistic Adaptations

 

A queen atop worker-built carton structure inside a Cecropia internode.

Workers harvesting food bodies

Cecropia, the perfect host

Cecropia plants are pioneers, meaning they are the first to colonize sunny disturbed areas like treefall gaps. Sunlight is a rare resource in the rainforest so many plant species fiercely compete to outgrow one another. Cecropia is among the fastest of these species, putting out a new leaf-baring internode at its apex every one to four weeks (depending on the species). The fast growing internodes are hollow, providing a spacious, temperature-controlled refuge for Azteca colonies to nest within the tree. Internodes are easily entered through the specialized prostomata (mentioned above) and septa between internodes are often chewed to create a continuous cavity inside the length of the stem (7). The spongy, white parenchyma tissue lining new internodes is nutritious and can also be used to create additional organizational structures within the internodes (5).

In addition to a cozy shelter, the plant also serves a nutritious diet to their hard-working colony. At the base of each giant radial leaf where the petiole meets the tree stem, there is a hairy, specialized structure called a trichilium that pumps out Müllerian food bodies. These beautiful white ovoids, just bigger than an ant egg, perfectly fit between the workers' mandibles and are packed with nutritious glycogen (8). For a balanced diet, the plant also provides translucent, fat-rich pearl bodies at sites across the underside of the leaves (8)

Azteca, the gallant defender

In return for food and shelter, the colony acts as an effective defense system for their tree and significantly reduces herbivore leaf damage and competing vines (9, 10). Workers actively patrol the tree's stem and leaves 24 hours a day, guarding it against intruders. If they encounter an insect herbivore, they will quickly attack it with their sharp mandibles and lift their gaster to spray a chemical spray composed of iridoids (11). They often release an alarm pheromone that recruits nearby patrollers to the threat. Often, the intruder quickly retreats and escapes. However, specialized hairs on the surface of the plant work together with hooks on the ants' legs that increases grip strength, allowing them to anchor large prey like katydids or grasshoppers (12). Occasionally, the workers are able to immobilize and kill the intruder, chopping it into small pieces and storing them inside the tree for later consumption. Workers will also fiercely attack much larger herbivores like sloths and monkeys (and humans). They will climb on top of the intruder, boarding it by the hundreds in search of a soft, sensitive spot where they can sink in their mandibles.

Workers even respond to the tree's distress cues. When a patroller encounters fresh leaf damage, volatile chemicals released by the plant alert the ant that there was recent danger (13). The ant responds by doing a brief, agitated sweep search before dotting a chemical trail from the leaf, down the petiole, and into the nearest stem entrance. A pulse of workers file out, following the trail to the specific site of the damage to search for the culprit.

 In addition to being fierce warriors, Azteca are also diligent house keepers and gardeners. They clear dirt and bits of debris off the leaf surfaces which ensures maximum photosynthetic potential. Also, fast-growing vines often plague pioneer species and compete for their sunlight. When foreign plant material contacts the Cecropia tree, patrollers distinguish it from their host and attack it. Workers chew on the meristem until it dies and the vine falls from the tree (9). The colony can also fertilize its host. Nitrogen consumed by the ants is passed to the plant and can be found in its leaf tissue (14, 15). Colonies maintain refuse piles inside the internodes and it is likely the nutrients are absorbed there, but the mechanism is still unknown. 

Workers kill and feast on a grasshopper

Workers attacking an encroaching vine

The colony's internal "trash piles" may be a source of nitrogen for the plant

Unprotected tree: leafcutters harvesting Cecopia leaves

Protected tree: Azteca ants killing a leafcutter scout

 

An illustration of defense and communication

One reason ants destroy vines is to eliminate points of entry that can be used by intruders (16). For a well-maintained tree, an intruder will only have access to the plant where the central stem meets the ground. If a tree falls in a storm or a landslide, many intruders try to take advantage of the colony’s structural vulnerability.

Here, a jumping spider attack is shown in slow motion (400 f/s) on a fallen tree. The spider attempts to remove the worker from her tree, but the specialized hooks on the legs of the ant fasten her to the plant (12). A nestmate comes to the rescue, biting the spider's leg and forcing it to retreat. At the same time, the ants presumably release an invisible, short-range alarm pheromone that alerts idle nestmates to the situation one-by-one in an expanding circle. One idle ant is activated by a tactile signal from another worker. The ants pursue the spider across a leaf and out of frame.

 

The Symbiotic Ecosystem

 

A complex web of interactions

Once you dissect open a Cecropia tree and expose its internal compartments, you'll immediately notice that ants and plants are not the only players in this story. There is a complex web of organisms whose intricacies and interactions are still largely unknown.

One of the first things you may notice are the flat ovals that cling to the wall. These mealybugs and scale insects have straw-like mouth parts to suck sap from the phloem of the tree (7). Because sap has such a high carb-protein ratio, the insects need to consume a lot to get enough protein for a balanced diet. They secrete the unused carbohydrates as a rich, sugary liquid that the Azteca ants love. Ants protect and tend scale insects like cattle inside the internodes of the tree, making sure they have good feeding sites and culling the population to prevent damaging population outbreaks. 

Brood surround a "nematode pile" inside the internode

Another observation you may make is that the colony's brood are often placed around a chocolate-colored, bulbous dome. Upon inspection with a dissection scope, you can see this pile is host to a sea of writhing nematodes. Little is known about their function, but they have mouthparts consistent with bacteria-feeding nematodes (17). It's possible they may provide a hygienic service for the brood, but more experiments are needed. 

Microbes play a big role in the nests of many ant species (such as leafcutters), and this is likely also true in the Azteca-Cecropia system. Bacterial communities differ in richness and abundance in certain internodes and between different areas of the plant. A certain group of fungus called Chaetothyriales is abundant inside Cecropia trees, especially residing in the nematode and trash piles (18). The fungal species that make up these communities depend on the Azteca species rather than the Cecropia species. Currently, the functional significance of these communities is unknown, but the possibilities are endless - ranging from parasitic to mediating nutrient transfer between the colony and the tree. 

Phorid flies are attracted to the Azteca alarm pheromone and lay eggs on distracted workers (19). Their maggots can be found inside the internodes, rummaging through the colony trash piles.

The specific relationships between these groups have hardly been studied. Many other unknown organisms that await discovery are undoubtedly interacting inside of this symbiotic ecosystem. 


References

1. C. C. Berg, P. F. Rosselli, D. W. Davidson, Cecropia (New York Botanical Garden Press, Flora Neotropica, 2005), vol. 94.

2. J. T. Longino, A taxonomic review of the genus Azteca (Magnolia Press, Aukland, 2007).

3. J. Gutiérrez-Valencia, G. Chomicki, S. S. Renner, Recurrent breakdowns of mutualisms with ants in the neotropical ant-plant genus Cecropia (Urticaceae). Mol. Phylogenet. Evol. 111, 196–205 (2017).

4. D. W. Davidson, Cecropia and its biotic defenses. B. CC, Fr. Rosselli P, Ed. Cecropia. New York New York Bot. Gard. p, 214–226 (2005).

5. J. P. Valverde, P. Hanson, Parenchyma: a neglected plant tissue in the Cecropia/ant mutualism. Symbiosis. 55, 47–51 (2011).

6. D. L. Perlman, thesis (1992).

7. J. T. Longino, in Ant-Plant Interactions, C. R. Huxley, D. F. Cutler, Eds. (Oxford University Press, Oxford, 1991), pp. 271–288.

8. F. R. Rickson, Anatomical Development of the Leaf Trichilium and Mullerian Bodies of Cecropia peltata L . Am. J. Bot. 63, 1266–1271 (1976).

9. D. H. Janzen, Allelopathy by Myrmecophytes: The Ant Azteca as an Allelopathic Agent of Cecropia. Ecology. 50, 147–153 (1969).

10. E. W. Schupp, Azteca protection of Cecropia: ant occupation benefits juvenile trees. Oecologia. 70, 379–385 (1986).

11. A. Dejean, J. Grangier, C. Leroy, J. Orivel, Predation and aggressiveness in host plant protection: a generalization using ants from the genus Azteca. Naturwissenschaften. 96, 57–63 (2009).

12. A. Dejean et al., Arboreal Ants Use the “Velcro® Principle” to Capture Very Large Prey. PLoS One. 5, e11331 (2010).

13. A. A. Agrawal, B. J. Dubin-Thaler, Induced responses to herbivory in the Neotropical ant-plant association between Azteca ants and Cecropia trees: response of ants to potential inducing cues. Behav. Ecol. Sociobiol. 45, 47–54 (1999).

14. C. Sagers, S. Ginger, R. Evans, Carbon and nitrogen isotopes trace nutrient exchange in an ant-plant mutualism. Oecologia. 123, 582–586 (2000).

15. A. Dejean, F. Petitclerc, O. Roux, J. Orivel, C. Leroy, Does exogenic food benefit both partners in an ant-plant mutualism? the case of Cecropia obtusa and its guest Azteca plant-ants. Comptes Rendus - Biol. 335, 214–219 (2012).

16. D. Davidson, J. Longino, R. Snelling, Pruning of host plant neighbors by ants: an experimental approach. Ecology. 69, 801–808 (1988).

17. A. Esquivel, J. Abolafia, P. Hanson, A. Pinto, A new species of Sclerorhabditis neotropicalis sp. n ( Rhabditida), associatedmwith Azteca ants in Cecropia obtusifolia. Nematropica. 42, 163–169 (2012).

18. M. Nepel et al., Ant-cultivated Chaetothyriales in hollow stems of myrmecophytic Cecropia sp. trees - diversity and patterns. Fungal Ecol. 23, 131–140 (2016).

19. K. a Mathis, S. M. Philpott, R. F. Moreira, Parasite Lost: Chemical and Visual Cues Used by Pseudacteon in Search of Azteca instabilis. J. Insect Behav. 24, 186–199 (2011).