Cheaters in the soil: The ecology and evolution of Indian pipes

indian-pipesIn early August this year, beneath the deep shade of old growth sugar maples, white pines, and northern red oaks in the teaching forest on my campus, Indian pipes were standing as translucently white as the finest candles. With their flowers nodding toward the forest floor, they looked like the clay pipes smoked by 17th century Dutch burghers. Over the next few weeks, the cellulose fibers in their stems shrunk and lifted the flowers skyward while the drying petals blackened and peeled away, exposing the football-shaped pistil surrounded by a wreath of stamens. By September, the plants had shriveled and become soot black, like the scrapings from one of those clay pipes. The miniscule seeds, tiny as dust, were dispersed after the blackened and dried ovary split open.

At a first glance, Indian pipes may seem like some sort of odd mushroom but they aren’t (they do, however, have a (literal!) connection with fungi – more on this in a moment). The Latin name for Indian pipes is Monotropa uniflora, which must be one of the more mellifluous Latin names given to any organism. Monotropa includes four other species found worldwide, all in northern regions. All of these species are in the family Ericaceae, which also includes blueberries, huckleberries, and wintergreen, among many others. Indian pipes and all of its near relatives in Monotropa lack chlorophyll but their more distant relatives – the blueberries, huckleberries, wintergreen, and other species in the Ericaceae – are all chlorophyllic and photosynthetic.

So, how do Indian pipes get the energy and nutrients they need to grow if they lack chlorophyll? Why have they lost their chlorophyll while their blueberry, huckleberry and wintergreen relatives retained theirs? How botanists have figured this out is a story that begins almost two hundred years ago.

Indian pipes and the discovery of mycorrhizal fungi

As far back as 1821, William Hooker, the founder of Kew Botanical Gardens and father of Joseph Hooker, one of Darwin’s closest friends, wondered whether Indian pipes were parasitic on the roots of trees or whether they decomposed dead organic matter like true fungi (my source for this interesting tidbit of botanical history is the excellent Tansley Review in The New Phytologist by Martin Bidartondo). The obvious way to answer this question is to dig up some Indian pipes and trace their roots to see if they are connected with tree roots. Because the roots of Indian pipes are thin and short, this is easier said than done. By 1842, after many attempts and much surprisingly heated debate, Thomas Rylands found that the roots of Indian pipes were not connected to roots of trees or shrubs but to the spider-silk fine hyphae of fungi instead. By the late 1800s, and after much exquisite but painstaking microscopic work, Franz Kamieński found that the fungal hyphae were also connected to the roots of woody plants as well as to Indian pipes. These fungi are now known as mycorrhizal fungi. Many, if not most, of the “mushrooms” you see on a walk through a forest are the fruiting bodies of vast networks of mycorrhizal hyphae.

The connections of the fungal hyphae and roots of green plants enable them to exchange carbohydrates and nutrients in a mutually beneficial symbiosis. The hyphae of mycorrhizal fungi take up water and nutrients from the soil and pass them along to the roots of trees and shrubs. From there, they are transported up to the green leaves high in the canopy where they support the machinery of photosynthesis. At the same time, carbohydrates produced by photosynthesis in the green leaves flow down the stem and into the fungi. Green plants and mycorrhizae therefore exchange carbohydrates and nutrients in opposite directions and to their mutual benefit.

Several individual trees or shrubs can be connected to the same hyphal network, which can spread over a hectare or more. Without these connections with mycorrhizae to obtain nutrients, most woody plants would die before they grew past the seedling stage of their life cycles. Little did Hooker suspect that his question about Indian pipes would, by the end of the century, lead botanists to discover an ecologically important but previously unknown symbiosis between fungi and woody plant species.

But back to Indian pipes. Indian pipes do not have much of a root mass of their own and so must rely even more heavily on the hyphae of mycorrhizal fungi, particularly of the genus Lactarius (milk-cap mushrooms) in the family Russulaceae, to obtain nutrients from the soil. Because Indian pipes did not have chlorophyll, botanists began to suspect that Indian pipes obtained both their carbohydrates and nutrients from the mycorrhizal fungi, the carbon coming ultimately from the leaves of the tree or shrub up the line. The best way to test this is to trace the amounts of rare isotopes of carbon and nutrients in woody plants, the fungi attached to them, and the Indian pipes. The changes in concentrations of these isotopes in woody plants, fungi, and Indian pipes tell us the direction they flow. Work of this sort by Eric Björkman and by Steve Trudell and his colleagues does indeed show that Indian pipes get their nutrients directly from the fungi and their carbon indirectly from the woody plants which are connected to the same hyphal network. Unlike the symbiosis between mycorrhizae and green plants, both carbohydrates and nutrients are flowing into Indian pipes from the mycorrhizal hyphae.

We now have an answer to Hooker’s original question about whether Indian pipes are parasitic on tree roots or are decomposers like true fungi. The answer is neither: they are parasitic on the symbiosis between woody plants and mycorrhizae, obtaining their carbon and nutrients only because the symbiosis exists at all. In a sense, the Indian pipes eavesdrop on the cross-exchange of nutrients and carbohydrates between fungi and woody plants.

Indian pipes are a plant that seems to form a third level of carbohydrate flow in a food chain from woody plants to fungi to Indian pipes, like the infield combination Tinkers to Evers to Chance in the old Chicago Cubs. On the other hand, Indian pipes are only the next level above the fungi with respect to the flows of nutrients. Because Indian pipes don’t easily fit into any of the traditional plant-herbivore-predator levels of food chains, they pose a real challenge to food web and evolutionary theory.

How did Indian pipes lose their chlorophyll?

Some recent DNA evidence compiled by Martin Bidartondo indicates that Indian pipes and wintergreen, its closest green relative, share a common ancestor. It is reasonable to assume that this common ancestor formed a symbiosis with mycorrhizae, as wintergreen does today. At some time in the distant past, one plant in this ancestral population mutated and lost its chlorophyll, becoming white as a consequence. Without chlorophyll, the white mutant could not make carbohydrates to grow and produce seeds. The carbohydrates had to come from the non-mutant green plants which remained attached to the same hyphal network.  The mutation not only caused the white plant to loose chlorophyll, it also reversed the direction of carbohydrate flow: carbohydrates now flowed into the Indian pipe’s roots from the fungal hyphae instead of flowing into the hyphae as with the green plants. The mutant ancestor of Indian pipes therefore defected from the mutually beneficial symbiosis with mycorrhizal fungi. Descendants of this mutant defector eventually evolved into Indian pipes and the other species in the genus Monotropa.

There is a technical term for this sort of mutation in evolutionary theory, namely, “cheater”. A cheater is an individual with a mutation that decreases its reproductive fitness but which benefits from other individuals without that mutation. The white ancestors could not produce seeds on their own, but only if they obtained carbohydrates through the mycorrhizae connecting them with their green relatives. Any population can withstand some small burden of cheaters, but not much. The cheater strategy is probably one reason why Indian pipes are relatively rare.  How did this cheater strategy come about and what were the selection pressures that made it so? No one seems to know.

Continued evolution since the appearance of this mutation has caused the Indian pipes and the wintergreens to diverge from their common ancestor. But the two plant species may have coevolved while remaining connected through shared mycorrhizae. No one seems to have found a mycorrhizal connection between Indian pipes and wintergreen, but it is entirely possible. From northern Minnesota to Nova Scotia, Indian pipes are most common in the same old growth North Woods forests where wintergreen also grows. I cannot recall ever seeing Indian pipes intermingled with wintergreens in any old growth forest, but if anyone has seen this please let me know: you may have a rare opportunity to determine if Indian pipes are cheating on a taxonomic cousin.

Population dynamics and conservation of Indian pipes

The sustainability of Indian pipes depends not only on the details of their parasitism on the woody plant-mycorrhizae symbiosis but also on seed production, mortality rates, and other population processes. As far as I can find in the literature, virtually nothing is known of the population dynamics of Indian pipes or of any other Monotropa relative. Several years can go by between blooms of Indian pipes in the same area; it’s been six years since I saw Indian pipes blooming in the teaching forest on my campus. What causes an entire population to go dormant for several years? Are the Indian pipes responding to differences in the weather from year to year? This year, I found them only in one of several nearby spots where I had seen them six years ago, so weather probably isn’t the only factor that determines whether they will bloom, otherwise they would have bloomed in all these places. Do Indian pipes bloom only in years of good growth of the green plants connected to them through their shared mycorrhizal network? Do the seeds remain viable in the soil for this long without decomposing and, if so, what protects them? Do the Indian pipe’s roots become dormant for several years?

Worthy questions all, but difficult to answer. Doing so will require a long-term research program patiently waiting for those bloom years as well as the continued preservation of old growth forests where Indian pipes are most abundant. The acreage of old growth forests, however, is declining slowly but steadily, partly because old growth forests are either harvested or burned in forest fires and partly because we are not letting younger forests grow older. Aldo Leopold once said that the highest value of wilderness and preserves is that they can be land laboratories where we can study how nature works. Studying the ecology and evolution of Indian pipes is not a bad reason to preserve and sustain old growth northern forests.

For Further Reading

Bitondardo, M. 2005. The evolutionary ecology of myco-heterotrophy. The New Phytologist 167: 335-352.

Björkman, E. Monotropa Hypopitys L, — an epiparasite on tree roots. Physiologia Plantarum 13: 308-327.

Leopold, A. 1941. Wilderness as a land laboratory. The Living Wilderness 6:3. Reprinted in S. L. Flader and J.B. Callicott, editors. 1991. The River of the Mother of God, and other essays by Aldo Leopold. University of Wisconsin Press.

Trudell, S.A., P.T. Rygiewicz, and R. L. Edmonds. 2003. Nitrogen and carbon stable isotope abundances support the myco-heterotrophic nature and host-specificity of certain achlorophyllous plants. The New Phytologist 160: 391-401.

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