by Liam Heneghan
Several years into my first large-scale field experiment, I noticed one of the technicians urinating on my experimental plot. It was a significantly worse event than when a cow inserted a hoof into one of my mesocosms in an adjacent part of the Co Kilkenny spruce plantation where I was working. The bovine mesocosm disaster was relatively inconsequential. The mesocosm was an isolated fragment of soil surrounded by PVC walls, open on top and with a collecting vessel below; it allowed me to examine the flow of nutrients through the earth. The hoof merely took one hoof-sized replicate of many out of play. The urination event was more significant; we might have to consider bottling his nitrogen-rich fluid for later analysis and factor it into the work. The technician and his urine had become an experimental treatment, quite an anomalous state of affairs.
The field experiment was a long-term evaluation of the effects of chemical additions, including nitrogen, on soils in a Kilkenny spruce plantation. After a brief interrogation about the technician’s en plein air habits, we were confident that, though several patches of the forest had enjoyed the benefits of his impromptu fertilization treatments, it seemed unlikely that the experimental plots had done so more than on this one occasion. A back-of-the envelope calculation confirmed that this small nitrogen addition was insignificant compared with the 150 kgs of nitrogen per hectare that we were adding to these plots annually.
Although the minor urination event, it turned out, was rather non-calamitous, my fieldwork was related to an investigation of a larger nitrogen calamity: a global experiment that I will call here the Great Urination Event (GUE), which has significant effects on biological diversity, on soil and water quality, and on human health.
Our work back then in the Kilkenny forest was conceived as an effort to evaluate the effects of components of “acid rain” on soil critters and soil processes. Acid rain is a general term for precipitation that is unusually acidic (because of the carbon dioxide in the atmosphere rain is “naturally” mildly acidic). Emissions of sulfur dioxide and nitrogen oxides chemically interact with water in the atmosphere to produce sulphuric and nitric acid which then rain down upon us. Like many human impacts on the environment, our activities are grafted onto natural processes, thereby greatly exacerbating their impacts on a wide variety of parameters. The effects of acid rain include damage to buildings, adverse effects on ground water and aquatic ecosystems, contributions to forest dieback (so-called “Waldsterben”), and implications for soils.
So why study acid rain’s effect on soil arthropods? These animals, typically microscopic, play a significant role in the regulation of soil processes, such as those that determine the release of nutrients from dead organic matter in the soil (e.g. dead leaf litter) needed for plant growth. If these communities were affected by acid rain then this, in turn, would have implications for key soil processes and ultimately for the plant community. The big “innovation” in our work was that we were convinced that much of the impact reported from acid rain studies came not from the acidity of the experimental treatment, that is, from the extra hydrogen ions in the rain (high acid = high hydrogen ion (proton) content), but rather came from the fertilizer effects derived from the sulfur and nitrogen in the precipitation (typically in Ireland, at least, as rain). This was the suggestion of my supervisor, Dr. Thomas Bolger, from University College Dublin. Thus our experiment examined the effects on soil animal of a range of nitrogenous and sulphuric components, some of which are highly acidic, but, importantly, others which are not. Furthermore, we asked if changes to the animal community indirect affected soil processes that ultimately influence all aspects of an ecosystem. And yes, these soil animals were affected in different ways by different fertilizer and acid treatments, which, in turn, affected other ecosystem properties.
Forgive me for writing a couple of longish paragraphs on this – the work described in the lines above encapsulate about six-years of my work life. I used to claim that ours was the last funded study on acid rain in Europe. Not true, of course, in a strict sense. I note with interest, though, that reference to “acid rain” in the title of research papers has greatly diminished over the past twenty five years. In 1985 one hundred and thirty five papers had the term in the title, in 1990 this was the case seventy-one times, 1995, forty-one times, 2000, twenty-seven times, 2005, twenty-four times, 2010, twenty-seven times, and six times so far in 2011. Incidentally, I got my PhD in 1994, just at the time when the term was losing its appeal. Had I been more attentive to such things back then I might have secured a full-time faculty position earlier.
Part of the reason for a diminishment in the use of the term “acid rain” recently relates to our greater regulation of the release of sulfur into the atmosphere from coal-fired power plants and from the implementation of other sound environmental policies. Nevertheless, relaxing of our attention to the issue does not mean we “solved” this problem. The rain remains acidic, and, in particular, our radical alteration of Earth’s nitrogen cycle, an especial contributor to the phenomenon, remains striking.
These days I am not just interested in the effects of added nitrogen on soil critters; I am interested in how disruptions to the nitrogen cycle associated with the Great Urination Event can have implications for the conservation of biological diversity.
Nitrogen, a primer
A short primer on nitrogen and its ecological importance: just the basic facts. Nitrogen is a “limiting nutrient”, the more you add (up to a point at least) the more things grow. It’s the reason we add fertilizers to our vegetable plots; it is also one of a number of reasons why humans eat. Like afternoon cocktails, nitrogen has certain uses but one can overdo it without planning to. You start with a couple and before you know it you’ve offended the dean (another story). Nitrogen fertilizes, and repeated applications can be excellent for a few target plants (like our lettuces), but after a certain point it can result in lowered plant diversity. So nitrogen can be good for the garden; it may not be so good in the lands we set aside for rest of nature. Nitrogen is the most ironic of the elements. It is why consideration of nitrogen is important for conservation – alas, not many conservationists think about the implications of disruptions to elemental cycles for conservation. We are hoping to remedy this.
So, nitrogen: the primer:
Nitrogen is a prevalent atmosphere gas; molecular dinitrogen is 79.1 per cent of the atmosphere’s volume. It is extremely stable in the atmosphere, and yet crucial for living things (for instance, for its use in proteins). Because of its molecular stability in the atmosphere, nitrogen is energetically expensive to coax into a form readily available in the biosphere. Two ways to make this happen prevail in nature: nitrogen can be “fixed” (converted to forms which can then enter the biosphere or the soil) either physic-chemically by means of lightning, ultraviolet irradiation, and combustion, or biologically by microbes (collectively called diazotrophs). Diazotrophs fix nitrogen, introducing nitrogen into the biosphere and into the soil where it becomes available for other organisms. They do so, not out of the goodness of their little microbial hearts, but to satisfy their own nitrogen needs.
These days nitrogen is industrially fixed by a process called the Haber-Bosch method at rates approaching that of microbes and lightning (some authorities suggest that all mechanisms considered, we now fix more that is fixed by natural pathways). The fixed nitrogen is used in fertilizers which ultimately produce much of our food (every mouthful that we consume is flavored with lashings of industrial nitrogen). Just as it is energetically expensive for microbes, fixing nitrogen is also energetically costly for us. So much fossil fuel is used to complete the process that many have quipped that ultimately we eat petrol and natural gas. Spreading nitrogen on soils as fertilizer in excess of plant productivity needs leads to nitrogen leakiness from agricultural soils, with consequences for the fouling of waterways (“eutrophication” is the term used for this). We have increased the spatial scale over which inorganic nitrogen gets distributed, leading to a significant loss of nitrogen in some areas, and “saturation” of nitrogen in the soils of other. Nitrogen in excess of habitual levels can have impact on biological diversity in our conservation lands, which, in some circumstances, leads to accelerated unraveling of communities of biological conservation concern.
To complete the cycle, nitrogen is lost from soil and returns to the atmosphere by a number of routes. It can outgas from the soil under several circumstances; often the nitrogen is lost as a consequence of microbial activity: bacterial going about their metabolic business can preside over the release of nitrogen back into the atmosphere. Other routes include the burning of organic material, including fossil fuels. Most will be familiar these days with the implications of burning of fossil fuels for the release of carbon dioxide, a primary gas implicated in human-caused climate change. When we burn ancient organic matter other gases are also volatilized, including nitrogen oxides. These nitrogen oxides are those that can react with water molecules in the atmosphere eventually creating the acid rain that falls upon us, bathing us in a nitrogen piddle of our own creation – the Great Urination Event.
We are living in the constant drizzle of excess nitrogen. And even when it is not drizzling on us, anthropogenic nitrogen deposition settles on us in a dry form like stardust, though somewhat less poetically.
The GUE, invasive species, and soil ecological knowledge
More can and should, and will be said about nitrogen in all its facets: more about its gaseous inertness in its molecularly doubled, triple-bonded form, in the atmosphere; more on its disinclination, without the energetic coaxing of the lightning spark or microbial processes, to “reduce” and make its way into the soil; of its indifference to the co-rivalry of root and fungal hypha; of its immobilization in organic matter and subsequent mineralization from decay; of its subsequent mobilization into the brownish and aquatically-lined matrix of the soil; of its myriad routes, either the rapid ones, or after long impediment in macromolecular humic compounds, back towards the sky.
I am considering having the nitrogen cycle tattooed on my children – it is just that important.
Much to say, but I take just one strand; one story of nitrogen and the vexations it creates under our poor governance. One of the ways in which we have inadvertently caused mischief with nitrogen is through our facilitated spreading of invasive species. Invasive species are those species that are transported by the humans either accidentally or on purpose beyond their native range into a new biogeographical region. Often the spread of species has minor ecological implications, but it can, in some circumstance, have significant consequences for the nitrogen cycle.
For instance, the introduction of fayatree (Myrica faya) to young volcanic soils in Hawaii was highly deleterious, since microbes in the roots of this tree can fix nitrogen, introducing this novel ecological function into the state of Hawaii for the first time with the result of creating an “invasional meltdown”, whereby the introduction of one species clears the way for the invasion of others and indigenous species go missing. Those species ushered in on the nitrogenously ample coattails of fayatree include non-native earthworms which, in turn, affect the nitrogen distribution which can encourage further changes in the vegetation. Another example, Acacia saligna in the South African fynbos (a system with exceptional bidiversity) is having very significant impacts on the vegetation in the historically low fertility soils of that region. In a study conducted in Cape Cod, Betsy Von Holle (University of Central Florida) and her colleagues found that plots invaded by Robinia pseudoacacia, black locust (a small tree more familiar to many readers, perhaps), appear to be associated with a proliferation of weedy, nonnative species.
Now, I choose this strand of the nitrogen story, not to provoke a debate about the wisdom of removing non-native species (in many cases, for the record, I think it is wise to do so). Rather, I am hoping that it illustrates that the ecological dimension of our nitrogen problems is not just that what we send up in the sky dribbles back down on us in a more caustic form (that is, the more conspicuous part of the Great Urination Event), it is also that we have rearranged the nitrogen cycle in a way that affects things as seemingly subtle as the distribution of organisms on regional scales. Thus, the GUE can interfere with the conservation of our biological resources.
Over the past decade my research has switched from the deposition phase of the Great Urination Event to investigations of the conservation biology subtleties associated with changes in the nitrogen cycle. Our model plant is Rhamnus cathartica, European buckthorn. This small tree is a relative rarity in its native Eurasian range. In Ireland, my own native range, buckthorn is confined, according to my copy of Webb’s “An Irish Flora”, “to rocky places and lake shores; occasional in the West and Centre, very rare elsewhere.” In the Chicago Wilderness region it is the most common woody species. Unlike fayatree or Acacia saligna, or Robinia pseudoacacia, buckthorn is not a nitrogen fixer; it does not form associations with microorganisms that incorporate atmospheric nitrogen into the soil. And yet there is mounting evidence that where it is persistently present, buckthorn is associated with an accumulation of nitrogen in the upper centimeters of the soil. This ostensibly small change is hypothesized to have some grave consequences.
A clue to why nitrogen accumulates under thickets of buckthorn came from an observation that undergraduates Cynthia Brundage, Constance Clay, and I made several years ago that the leaves of this small tree are high in nitrogen compared to other native trees in the systems that it invades. The high nitrogen in the leaf litter translates into a rapid breakdown of leaves in invaded woodlands; in fact, buckthorn leaf litter appears to drag the leaves of other species along with it, to the point that quite regularly, soils under buckthorn thickets are quite shamelessly devoid of a modest coverlet of leaf material. The nude soil is susceptible to rapid erosion and perhaps more seriously, since a huge diversity of life is found in those upper centimeters of the soil, there may be a massive loss of these species as a result of the invasion of this rare European tree. This latter phenomenon may amount to a local mini mass-extinction of soil organismal diversity. And if this is not complicated enough, buckthorn invasion is associated with an invasion of Eurasian earthworms. Much of the upper Midwest in the US does not have native earthworms; all the earthworms are relatively recent introduced. Put another way, if ever you slid on an earthworm on a moist spring afternoon on a Chicago sidewalk, the mucous you scraped off your shoe was probably that of a European lumbricid worm. Earthworms, in turn, change aspects of the nitrogen cycle and so forth in a spiral so complex that all these events, buckthorn invasion, litter loss, arthropod decline, earthworm advance, modified soils, nitrogen enrichment, corkscrew through the region to create a conservation problem that will not be easily fixed. Conjectures about buckthorn invasion in the midwest are being worked out in detail by PhD students Basil Iannone and Lauren Umek.
Attempts to remediate the sort of problems associated with invaders are typically disconnected from a consideration of the Great Urination Event. Although the field of restoration ecology and restorative management is becoming increasingly sophisticated and effective, nevertheless, human intervention on behalf of returning a system to a measure of ecological health often proceeds without direct regard for the way in which soils have been modified by a suite of invading species. The assumption might be that soils will passively follow the plant community, whereas it may be that a return to ecological good fortune requires us precisely to go the other way – start with this soil! Some colleagues and I have named the approaches to conservation problem solving that start from the ground up Soil Ecological Knowledge Systems (SEKS; the adjective is, of course, SEKSy).
As SEKSy as Mulch!
Of course, it does not get SEKSier than mulch! Mulch, typically defined as organic material used as a covering on soil, is ordinarily applied to retain moisture, to suppress weeds, and often to add nutrients to soil. It may seem somewhat counterintuitive to suggest that mulch might be usefully deployed to remediate the GUE. The argument goes as follows. In fertile soils, nitrogen levels are greater than they are in organic mulches, especially woody mulches. Wood is primarily cellulose, lots of carbon, relatively little nitrogen. When applied to a fertile soil the microbes come running like kids to a piñata. In order to utilize the wood they need nitrogen for growth, and since most microbes cannot fix nitrogen from the atmosphere they satisfy their nitrogen requirements by importing it from the soil surrounding the decaying wood mulch thereby immobilizing it, and leaving less available for plants (recall: nitrogen’s “indifference to the co-rivalry of root and fungal hypha”). Although this nitrogen is not taken out of ecosystem circulation indefinitely, nevertheless it can reduce fertility enough to allow for native plants communities to re-establish themselves. It is still early days in research on mulch (or other carbon additions) as a way of remediating the GUE. Sometimes it works, sometimes not. How much to add; when to add it; what should the mulch be comprised of? It is not clear. And, of course, mulch is one of the more exotic ways of dealing with excess nitrogen. I mention it only becuase it is a method that connects GUE with the conservation issues that currently interest me. We need to carefully manage both nitrogen input as well as the effects of excess inputs. This management issue will remain as significant an challange for us as climate change in the coming decades.
Putting this all together it looks like this: Human modification of nitrogen cycle on a global scale is a less apparent component of global change than climate change, or massive shifts in land use, or the intercontinental swapping of species. On the one hand it is impressive: in a manner that only some plucky microbes have been able to in the past, we have modified the cycling of a vital element on a planetary scale. But such achievement comes at a cost. When the nitrogen is farted back into the atmosphere, it is converted there into nitrogenous fluids that drizzle back upon us – the conspicuous phase of the Great Urination Event. Internal, less conspicuous, changes in planetary metabolism, ofter derived from other aspects of global change, can create unforseen consequences. Interaction between aspects of global change, for instance, modifications of the global nitrogen cycle and the spread of invasive species exacerbate the patterns of both in ways that are exciting for scientific research but mischievous when it comes time for a cleanup. A suite of remediate techniques have been proposed.
Today’s GUE suggestion: bring an umbrella.
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[Photos in order: Gents (by Randall Honold); Pissoir (by Randall Honold); 2 N books and a flora (Heneghan), Oppiella nova (approx 0.5 mm length) (by Claire Gilmore and Heneghan) Mulch pile reseach team (left to right Heneghan, Kim Frye, Lauren Umek, Will Warner, Chris Mulvaney).]
Heneghan, L, Miller, Susan P; Mac A Callaham Jr; Baer, Sara; Montgomery, James; Richardson, Sarah1; Rhoades, Charles C; Pavao-Zuckerman, Mitchell (2008) Integrating a soil ecological perspective into restoration management. Restoration Ecology 16 (4): 608-617.
Sprent, J (1978) The Ecology of the Nitrogen Cycle Cambridge Studies in Ecology. Cambridge University Press, Cambridge.
Stevenson, F. J., M. A. Cole (1999) Cycles of Soil: carbon, nitrogen, phosphorus, sulfur, micronutrients. John Wiley and Sons, New York.