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.