Freeloading caterpillars get in the way of plant-ant mutualism

Cecropia obtusifolia provides food for ants that come and protect it—unless caterpillars get there first. Photo by wallygroom.

ResearchBlogging.orgImagine you need a team of security guards. To find them, you decide not to place an ad in the local paper or on Craigslist. Instead, you build an apartment complex next to your home, complete with a full-service cafeteria providing free hot meals 24 hours a day. You leave the front doors unlocked, then hope that anyone who shows up to live in the apartments will also keep an eye on your home.

If you took that strategy to protect your assets, you’d have to be crazy. But that’s pretty much what ant-protected plants do all the time. They grow hollow structures called domatia, secrete nectar from special structures, and even produce tasty and nutritious “food bodies.” Then they wait for ants to move into the domatia, eat the nectar and the food bodies, and hopefully chase away anything that might want to do the plant harm. The crazy thing is, it works.

Well, it mostly works.

One gap in the ant-protection mutualism is the period when an ant-protected plant hasn’t grown big enough to support a whole colony of ants. In this early stage, ants won’t colonize the plant, but other insects might be quite happy to take the rewards that are already being offered. That’s exactly what larvae of the butterfly Pseudocabima guianalis do—they make themselves at home on unprotected ant-plants.

The ant-plant Pseudocabima caterpillars target is Cecropia obtusifolia, a shrubby Central American tree that relies on ants in the genus Azteca for protection. Azteca ants make vicious and well-coordinated bodyguards. Here’s video Ed Yong posted last year, showing a bunch of the ants flushing a hapless moth into an ambush.

However, Cecropia saplings can’t produce enough food to support a colony of ants until the plants grow to more than a meter tall. What’s too little for thousands of ants is a feast for a Pseudocabima caterpillar, however. Each caterpillar builds a silk shelter around a region of the plant that grows food bodies, and settles in to eat. As it grow larger, the caterpillar moves into a domatium near its original shelter, covering the entrance hole with silk. Finally the caterpillar pupates inside the domatium, emerging as an adult to lay eggs on another unprotected Cecropia plant.

Eventually the Cecropia saplings grow large enough to attract ants, who run off the caterpillars. However, as the paper I linked to above describes, the caterpillars seem to be able to resist an ant colony’s establishment on the plant—the silk shelters prevent ants from getting to the best sources of food. Cecropia saplings occupied by caterpillars didn’t seem to suffer more herbivore damage than ant-protected plants, but they did grow more slowly over the course of several years’ observations. Caterpillar-infested Cecropia plants were also more vulnerable to infection by a fungus, which the ants removed quite effectively.

Interestingly, though, caterpillar-infested plants also produced less food than those guarded by ants. This is a point of circumstantial evidence for a new model of mutualism I wrote about earlier this year, in which cheating is reduced or prevented when a host like Cecropia better mutualists help create better rewards. An ant-protected plant can divert more resources to feeding its tenants, so their work rewards itself. However, Pseudocabima caterpillars are glad to take the lower level of rewards that Cecropia plants offer up to all comers.

In other words, if you’re going to give out free lunches, you can’t really expect everyone who eats to pay you back.

Reference

Roux, O., Céréghino, R., Solano, P.J., & Dejean, A. (2011). Caterpillars and fungal pathogens: Two co-occurring parasites of an ant-plant mutualism. PLoS ONE, 6 : 10.1371/journal.pone.0020538

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First step to mutualism doesn’t look so friendly

This post was chosen as an Editor's Selection for ResearchBlogging.orgAnt-plant protection mutualism is a widespread and elegant species interaction. How do species strike bargain like this, requiring specialized behaviors and structures in each partner, in the first place? A new report in The American Naturalist suggests an answer: maybe ants took the initiative [$-a].

In exchange for protection from herbivores and competitors [big PDF], “myrmecophytic” host plants grow hollow structures called domatia and often produce nectar to shelter and feed a colony of ants. This mutualism is really a sort of negotiated settlement between the partners; both ants and plants do what they can to get the most out of the interaction. We have evidence in some cases that host plants cut back support for ants if there aren’t any herbivores around; and, in other cases, that ants prune their host plants to prompt the growth of more domatia.



Domatium diversity: Ant domatia on Acacia (above) and Cordia nodosa (below). Photos by Alastair Rae and Russian_in_Brazil.

So it isn’t entirely surprising that there might be cases where that bargain hasn’t been established yet, and that’s what the new paper reports. The observation turned up in connection with one of the most interesting forms of the ant-plant mutualism: the “devil’s gardens” of the Amazonian rainforest. Devil’s gardens are created by colonies of the ant Myrmelachista schumanni, which attacks possible competitors to its preferred host [$-a], Duroia hirsuta, leaving patches where nothing but D. hirsuta grows.

Clued in by native research assistants, the group studying the devil’s garden interaction discovered that trees growing at the edge of a garden are often afflicted with swollen, distorted trunks. Cutting into the swellings, they found them riddled with passages and populated by M. schumanni. The trees in question are not known as myrmecophytes, and it’s not clear that they receive any benefit from hosting ants. In fact, the authors report that ant-occupied trunks are weakened, and prone to breakage under their own weight or under heavy wind.

The paper doesn’t present direct evidence that the ants create the galls, but as the authors explain, this seems likely — M. schumanni kills its hosts’ competition by injecting them with formic acid, which parallels the irritants other gall-making insects inject into their host plants. It make sense that gall-making might have started as ants’ attempts to kill off trees that are too big to succumb to formic acid outright, but respond to it by growing galls like scar tissue. Furthermore — and this is pure speculation, of course — this looks like a first evolutionary step toward true ant-plant mutualism. Domatia may have originally evolved to redirect ants from more damaging gall-making, and since ants are naturally territorial about their nests, it might not take much behavioral change before they end up protecting their host.

References

Edwards, D., Frederickson, M., Shepard, G., & Yu, D. (2009). A plant needs ants like a dog needs fleas: Myrmelachista schumanni ants gall many tree species to create housing. The American Naturalist, 174 (5), 734-40 DOI: 10.1086/606022

Frederickson, M., Greene, M., & Gordon, D. (2005). “Devil’s gardens” bedevilled by ants Nature, 437 (7058), 495-6 DOI: 10.1038/437495a

Janzen, D. (1966). Coevolution of mutualism between ants and acacias in Central America Evolution, 20 (3), 249-75 DOI: 10.2307/2406628

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Ants trim trees for more living space

ResearchBlogging.orgIn the natural world, cooperative interactions evolve not as expressions of altruism, but as careful “negotiations” between interacting species. Each player may benefit from the relationship, but each stands to benefit from trying to cheat the other. In this month’s issue of The American Naturalist, we see a prime example: mutualistic ants sterilize their host plants [$-a] to get the most out of the interaction.



Cordia nodosa flowers (top)
and ant domatia (bottom)

Photos by Russian_in_Brazil.

The ant species Allomerus octoarticulatus is part of a classic protection mutualism with the tropical tree Cordia nodosa, in which the plant grows structures called domatia that provide shelter for a colony of ants, and nutrient rich “food bodies” for the ants to feed on. The ants, in turn, patrol the plant and drive off herbivores. This mutually beneficial relationship also sets up a conflict of interest. The tree must divide its resources between providing food and shelter for its resident ant colony — growing new domatia and fruiting bodies — and its own reproductive efforts — growing flowers and fruit. The ants, naturally, would prefer for the host tree to spend as much energy as possible on them.

Indeed, Allomerus octoarticulatus has been observed killing the flowers of its host trees. This is what led the new paper’s author, Megan Frederickson, to conduct a simple experiment on C. nodosa, asking whether such pruning prompts the tree to grow more domatia. She experimentally removed flowers from trees occupied by a species of ants that don’t engage in flower pruning to see if pruned trees grew more domatia — and pruned trees grew more domatia over the course of four months than trees that were allowed to flower and produce fruit.

Ant-hosting plants need not be totally subject to the whims of their protectors, however — this kind of regulation works both ways. A study published last year in Science found that ant-hosting Acacia trees cut back on support for their resident ant colonies [$-a] when herbivores are removed and ant protection is no longer needed. (I wrote about this study back when it was released.) It seems likely that flower-pruning ants are exerting strong selection on Cordia nodosa to circumvent this behavior — a new tree variant that can overcome pruning, or make life uncomfortable for pruning ants, should have a large selective advantage.

In the absence of such a mutation, as Frederickson points out, Allomerus octoarticulatus is creating a tragedy of the commons by reducing the long-term viability of its host tree’s populations in exchange for the short-term benefit of more living space. As it stands, Cordia nodosa can only reproduce when it hosts non-pruning ant species, which are a minority in the populations Frederickson studied. Only time, and further study, can determine whether this mutualism might break down altogether.

References

Frederickson, M. (2009). Conflict over reproduction in an ant-plant symbiosis: Why Allomerus octoarticulatus ants sterilize Cordia nodosa trees. The American Naturalist, 173 (5), 675-81 DOI: 10.1086/597608

Palmer, T., Stanton, M., Young, T., Goheen, J., Pringle, R., & Karban, R. (2008). Breakdown of an ant-plant mutualism follows the loss of large herbivores from an African savanna Science, 319 (5860), 192-5 DOI: 10.1126/science.1151579

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