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Are ants' fungus gardens a source or sink for nitrogen?

This week's paper, Symbiotic Nitrogen Fixation in the Fungus Gardens of Leaf-Cutter Ants, has already been discussed by Ed Yong, whose blog is among my favorites, and by the always-interesting Susan Milius of Science News. When she interviewed me, I endorsed the main conclusions of the article but expressed skepticism on one point.

The paper clearly shows that the fungus "gardens" cultivated by leaf-cutter ants contain bacteria that extract nitrogen from the air. The part I wondered about was their statement that:

We estimate that a single mature leaf-cutter ant colony may contribute as much as 1.8 kg of fixed N per year into neotropical ecosystems (see SOM text for details).
The ant colonies are part of the ecosystem, so I guess nitrogen the colony contributes to itself is a contribution to the ecosystem, just like profits made by currency speculators are a contribution to the economy. But are the ant colonies a source of nitrogen for neighboring plants, or are they taking nitrogen from those plants?

Page 14 of the Supplementary Material presents estimates from a paper by Wirth and colleagues showing that the ants harvest leaves containing 18 grams of nitrogen each day, and discard 12 grams of nitrogen (used-up leaves, etc.) in refuse piles. They estimate that 4.9 grams of that discarded nitrogen comes from the nitrogen-fixing bacteria in the ants' fungus garden, but so what? They are still taking 6 grams more nitrogen from the plant community each day than they are returning.

Before we can decide whether ant colonies are a source or a sink of nitrogen, we need to know what happens to the 6 grams of nitrogen that apparently disappears into the ant colony each day. When ants defecate away from home, that could return some nitrogen to the plant community, a contribution not included in the calculation above. Nitrogen that accumulates within the fungus garden may eventually become available to plant roots when the nest is abandoned. But some nitrogen in the ant colony may be permanently lost from the ecosystem. This includes gaseous losses as ammonia or nitrogen oxides. Nitrate nitrogen can move down into the soil with percolating water; some of this leached nitrogen may be recaptured by roots before it gets too deep in the soil, but the rest will be lost, eventually reaching a river or ocean.

Until we have more information on these processes, all we can say is that the colony appears to take more nitrogen from the plant community than it returns to them, despite the fact that the ants get some of their nitrogen from nitrogen fixation rather than importing all of it in harvested leaves.

Furthermore, the nitrogen they do return is distributed, not for maximum benefit to the plant community, but for the convenience of the ants. This reminds me of a feed lot that takes in grain-protein nitrogen from a large area, then dumps manure nitrogen in a small area at higher rates than plants can use.

There is also an interesting evolutionary question here. Why do the bacteria in the ant gardens fix nitrogen? Symbiotic rhizobium bacteria in the root nodules of legumes fix much more nitrogen than they need for their own growth and give most of it to their plant hosts. We showed that they do this because nodules that fail to provide their hosts with nitrogen are subject to sanctions that reduce the reproduction of rhizobia inside (Kiers et al. 2003); this prevents such "cheaters" from becoming too common. But I don't see how ants could impose sanctions on different bacterial genotypes based on how much nitrogen they fix. So my guess is that these bacteria only make as much nitrogen as they need for their own growth, and release it mainly when they die. Or, perhaps, when they are killed.

Kiers, E.T., Rousseau, R.A., West, S.A. & Denison, R.F. (2003) Host sanctions and the legume-rhizobium mutualism. Nature, 425, 78-81.

R. Wirth, H. Herz, R. J. Ryel, W. Beyschlag, B. Holldobler, Herbivory of leaf-
cutting ants. A case study on Atta colombica in the tropical rain forest of
Panama, Ecological Studies (Springer, Berlin, Heidelberg, 2003), pp. xvi, 230.

Comments

Ford:
I did see Susan's coverage of this paper and noted her interview of you. Are you becoming a rock star of science? I'll have to have to start telling folks "I knew him when..."

Anyway, you bring some great questions to the discussion and let's follow on to a couple.

Any nitrogen fixed by the bacteria in the nest would have to figure into the overall N budget of the ecosystem, regardless of who gets credit. I agree that the ant colony does not necessarily become an N source (for the specific reasons you cite) but without N fixing in the nest one can argue the nest would have to be an even stronger sink or would not be as significant a piece of the ecosystem. Figure this as something akin to opportunity cost. Of course one could expand this latter line of reasoning to suggest that the N fixing bacteria "enable" the nest to be stronger than it might otherwise be and as such have a bigger appetite for leaves and ultimately harvest more leaf N from the surrounding plants.

More fascinating to me is your later question about why in the first place do these N fixers occur in such unexpected concentrations in the nest. Are they "cared for" ala the fungus? I'm not sure sanctions are the only way a commensal can entice behaviors... a carrot vs. stick approach comes to mind. If the ants actively help N fixers in some way that corresponds to the amount of N fixed then by corollary they are not helping less beneficial bacteria (cheaters or even less effective fixers). This would build a selection scheme that evolution should reward.

These ant communities should provide a lot of opportunity to start teasing apart some fascinating ecology. I think there should be some future Science Fair projects with little leaf cutter ant farms (if there aren't some already).

Uh, Clem,

This is the second reporter who has asked me to comment on a paper about fungus-growing ants, so maybe my blogging gives the impression of broad expertise? Maybe "expertise" is too generous -- broad interests? I have been fascinated by this system since third grade, when my mycologist father took the family to Costa Rica on a field trip, and leaf-cutter ants ran regattas through our house.

I agree that the N fixation will, as a minimum, make the ant colony a weaker sink for N. Elsewhere, of course, ecologists are concerned that anthropogenic N deposition is reducing plant diversity, etc., so it's not clear that an N sink would necessarily be bad in all respects.

A smaller reward is the evolutionary equivalent of a fitness-reducing sanction; over a few generations, strains getting smaller rewards will be displaced by strains getting larger rewards. But I don't see how ants could tell that one bacterial cell (or a cluster of clonally identical cells) is fixing more N than another cell 0.1 mm away. Legumes have an easier task: measuring fixation by a 2-3 mm nodule, often containing a single genotype of nitrogen-fixing rhizobia.

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