Fires foster biological diversity on the African savanna

As an ecology student back in days of yore, I was introduced to the classic mutualism between ants and swollen-thorn acacia trees. In this mutually beneficial relationship, ants protect acacia trees by biting and projecting very smelly substances at hungry herbivores, and by pruning encroaching branches of plant competitors. In return for these services, acacia trees provide the ants with homes in the form of swollen thorns, and in some cases also provide food for their defenders.

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Swollen thorns of Acacia drepanlobium occupied by C. nigriceps. Credit: Ryan L. Sensenig.

I always assumed there were limits to what these ants could do. I knew that elephants were a constant problem for trees trying to get established on the African savanna. I figured, wrongly, that ants could not do much to counter a determined thick-skinned elephant. But as Ryan Sensenig describes, ants will swarm any intruding elephant, rushing into the elephant’s very sensitive trunk and mouth, biting it and, in some cases, exuding a chemical compound that is very offensive to an elephant’s keen sense of smell. So don’t mess with these ants if you can help it!

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The Laikipia Plateau has one of the few growing elephant populations in East Africa. Credit: Ryan L. Sensenig.

Fires play an important role in savanna ecosystems, killing many trees before they can get established, and creating a mosaic of burned and unburned areas which vary in grass quality and quantity, and in the abundance of acacia trees (and other species as well). Recently burned grasslands tend to be lower in grass abundance and higher in grass nutrient levels. In a previous study of controlled burns, Sensenig and his colleagues showed that larger animals, such as elephants, tended to graze in unburned areas, which had more grass – albeit of lower quality. Returning seven years after the burn, he was surprised to find that elephants, which eat both trees and grass, had shifted to the burned sites in preference to unburned sites. He thus wondered whether fire was having an impact on the ant-acacia mutualisms that defend acacias from elephants and other large herbivores.

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Sunset strikes an Acacia xanthophloea on Mpala Research Centre in Laikipia, Kenya. Credit: Ryan L. Sensenig.

Ants do not share trees. In Mpala Research Centre in the Laikipia Plateau of Kenya, there are four mutually-exclusive species of ants that live in Acacia drepanolobium trees: Crematogaster sjostedti, C. mimosae, C. nigriceps, and Tetraponera penzigi.

Sensenig and his colleagues wanted to know whether the controlled burns had a long-lasting effect on ant species distribution on acacia trees. The researchers surveyed 12 plots that had been burned seven years previously and an equal number of unburned plots to see how burns affected which ant species were present.

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Goshen College research students estimate ant densities on Acacia drepanolobium trees in the Kenya Longterm Exclosure Experiment. Credit: Ryan L. Sensenig.

They found that C. nigriceps was more common in acacias from burned areas while the other three species were more common in trees from unburned areas.

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Why were there more C. nigriceps ants in previously burned areas? One explanation is that perhaps C. nigriceps is better at avoiding getting burned by fire, or else is better at recolonizing after a fire. To look for species difference in response to fire, the researchers simulated fires by burning elephant dung and dried grass in 3-gallon metal buckets, creating a small sustained smoke source. They stationed observers every 50 meters along a 500 meter transect for the first experiment, and a 1.8 km transect for the second experiment. They then measured ant-evacuation rate by counting the number of ants moving down the trunk. There were some very pronounced differences, with C. nigriceps having the highest evacuation rate, C. mimosae also showing a strong smoke response, and the other two species showing little evidence of any response.

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Evacuation rate for each species in response to smoke.

C. mimosae generally prevails when it battles a colony of C. nigriceps. These results indicate that the subordinate C. nigriceps is able to maintain its presence in the community, in part, by taking advantage of its superior performance when it encounters a fire. The researchers also found some evidence that C. nigriceps is better at recolonizing after a fire than is C. mimosae. So despite being the subordinate species, C. nigriceps is abundant in this ecosystem.

Returning to those elephants, the researchers describe one final experiment in which some plots had a series of fences that excluded herbivores, while other plots were open to herbivores, including elephants.

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In this experiment, as well, there were burned and unburned plots. In general, there were more ants present when herbivores were present, as the trees invested more in swollen thorns and in ant food (in the form of nectar) to attract protective ants. In addition, ants were more abundant in unburned plots than in plots that had been previously burned, with the exception of C. nigriceps when herbivores were excluded.

Ecologists have long known that fire maintains savanna ecosystems by preventing the grasslands from being overgrown by trees. This study shows that fires shift ant community structure in favor of the subordinate ant species (C. nigriceps), resulting in a higher diversity of ant species overall. The researchers suggest that if fires become more common in savannas, elephants may become more attracted to acacias that harbor a reduced (or nonexistent) cast of defenders, which could lead to a further reduction in the abundance of acacia trees and their mutualistic ants.

note: the paper that describes this research is from the journal Ecology. The reference is Sensenig, R. L., Kimuyu, D. K., Ruiz Guajardo, J. C., Veblen, K. E., Riginos, C., & Young, T. P. (2017). Fire disturbance disrupts an acacia ant–plant mutualism in favor of a subordinate ant species. Ecology, 98(5), 1455-1464.Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.

Nitrogen nurses

Alfred Lord Tennyson puzzled over the conflict between love as a foundation of Christianity, and the apparent violence of the natural world.

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

The good poet would be relieved to learn that modern ecologists have uncovered a softer, gentler side of the natural world – facilitative interactions, in which one species (the facilitator) helps out a second species. In many, but not all, cases, the second species also helps out the first species. Ecologists describe these mutually-beneficial interactions as mutualisms. As an example, Mimosa luisana is a mutualist with Rhizobium bacteria, providing the bacteria with root nodules to live in and carbohydrates as an energy source, while receiving ammonia (NH3) that the bacteria fix (convert) from atmospheric N2. A second type of mutualism, a mycorrhizal association, is a very common facilitative interaction between plants and fungi, which grow alongside or within the plant roots. In many mycorrhizal associations, the plant provides carbohydrates to the fungi, which import and share nutrients and water.

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Mimosa luisana. Credit: Leticia Soriano Flores, algunos derechos reservados (CC BY-NC)

Alicia Montesinos-Navarro and her colleagues, and researchers before them, noticed that in arid and semi-arid environments, plant-plant facilitation was most common between two plant species that were structurally and functionally very distinct, and that tended to be very distantly related to each other. In particular, M. luisana tends to associate with many different species of plants, including many cacti that look nothing like it, and are very distantly related. M. luisana is called a nurse plant, because other species tend to grow under its branches, which shade the soil and reduce water loss from evaporation. Recent work by Montesinos-Navarro and her colleagues showed another benefit of nursing – some plants receive nitrogen from these nurse plants via the network of mycorrhizal fungi.

Traditionally, ecologists have argued that associations between distantly-related plants occur because the plants have very different ecological niches, using different resources in different ways, so they are not competing with each other. Montesinos-Navarro and her colleagues argue that a second process might be important in this and other systems. Close relatives of M. luisana might tend to have high nitrogen levels and thus not benefit from nitrogen transfer from the nurse plant, while more distantly-related plants might tend to have lower nitrogen levels and thus benefit from any nitrogen arriving from M. luisana. They explored this hypothesis in the semi-arid Valley of Zapotitlan in the state of Puebla, Mexico.

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Study site dominated by the columnar cactus Neobuxbaimia tetezo, Credit: Alicia Montesinos-Navarro.

Measuring nitrogen transfer from the nurse plant to the recipient is not the world’s easiest task. Fortunately there is a rare form or isotope of nitrogen, 15N, which can be distinguished from the more common 14N. The researchers soaked M. luisana leaves in urea that was made up of primarily 15N, and the leaves took up the urea. Consequently, any exported nitrogen would contain a disproportionately high concentration of 15N, resulting in high 15N levels in the recipient plant. They then measured 15N levels in 14 different species of plants that used M. luisana as their nurse. The researchers were able to test two hypotheses. First, they could see whether close relatives to M. luisana tended to have higher N-levels than more distantly related species. Second they could see whether distant relatives tended to receive more nitrogen from nurse plants than did close relatives.

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Mimosa luisana branch taking up 15N-labeled urea. Credit: Alicia Montesinos-Navarro.

The graph below summarizes the results. The y-axis measures how much the 15N level in the facilitated species increased by the end of the experiment (15 days). The x-axis measures the evolutionary relationship between M. luisana and the facilitated species – more precisely how long ago the two species shared a common ancestor. Lastly, the size of the dot measures the initial difference in leaf N-levels between M. luisana and the facilitated plant.

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Influence of evolutionary relationship between M. luisana and the facilitated species (x- axis) and nitrogen gradient – the initial difference in nitrogen levels between the two species (size of dots) on the amount of nitrogen imported by the facilitated species.

Several trends are evident. First, close relatives of M. luisana tended to have similar leaf nitrogen values to M. luisana (medium sized dots), while distant relatives tended to have much less nitrogen than M. luisana (largest dots). Second, the most distant relatives tended to have the greatest increase in their 15N levels, which indicates that they received the greatest nitrogen export from their nurses.

One question is how the nitrogen is transported. Montesinos-Navarro and her colleagues describe how they treated soil with a fungicide, presumably killing the mycorrhizae, which resulted in a substantial reduction in nitrogen transport. This suggests that the mycorrhizal network is important for nitrogen transport. But more pressing is what do the nurse plants get out of the relationship. The researchers suggest that the recipient plants may provide M. luisana with either water or phosphorus, both of which may be in short supply in arid environments.

This study indicates that we need to look beyond traditional niche theory, and may need to  dig deeper to understand the structure of plant communities, and how facilitative interactions can explain the coexistence of very distantly related plants.

note: the paper that describes this research is from the journal Ecology. The reference is MontesinosNavarro, A., Verdú, M., Querejeta, J. I., & ValienteBanuet, A. (2017). Nurse plants transfer more nitrogen to distantly related species. Ecology, 98(5), 1300-1310. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.