Friday, September 21, 2012

Global N cycling: the Climate-Nutrient hypothesis

Patterns of soil 15N and P availability in the Amazon. From Quesada et al. 2010.

When we looked earlier, the degree of decomposition affects soil organic matter content and the isotopic ratio of the N in the soil.

For individual classes of organic matter, be in leaves, organic layers, mineral soils, or fractions of mineral soils, the more microbes process organic matter, the more C is lost and the more enriched the nitrogen becomes in 15N.

The "processing hypothesis" is a standard explanation for vertical profiles of organic matter in soils. Deep soils have lower C concentrations and higher del15N than shallow soils because the stuff at the bottom has been worked over by microbes**.

**Other mechanisms affect vertical profiles, too. Plants preferentially cycle light N up to the top. Illuviation can also transport C and N downwards.

What applies vertically, could also apply horizontally.

Yet geographic patterns have largely been explained with the fractionating loss hypothesis. Soils enriched in 15N are thought to be enriched because they have lost a larger proportion of their N to fractionating pathways compared to relatively depleted soils.

Two sets of observations come together to generate the main latitudinal patterns.

1) Tropical soils are enriched in 15N compared to temperate soils
2) Tropical soils have high rates of N2O flux.

Put together, the two reinforce one another to solidify a view of latitudinal gradients.

But why would that be?

Nitrification or denitrification are not thought to be temperature sensitive like nitrogen fixation.

Therefore, it's indirect controls.

One of the major hypotheses is the Climate-Nutrient hypothesis. Tropical systems are thought to be more P-limited, which increases the degree of N surplus. Greater N availability increases the likelihood of gaseous N loss.

Quesada's work (above) is a good example of data that calls this hypothesis into question.

Within the Amazon (which is all hot), across a gradient of P availability, 15N is lowest in low P soils, not high P soils. Low P soils are supposed to have the greatest excess N and the most gaseous N loss.

To maintain the Climate-Nutrient hypotheses, explanations get pretty complicated. Rates of N2-fixation by plants have to vary in ways that one wouldn't expect. Or losses have to become episodic and almost catastrophic. 

A number of other questions come up. Recent work suggests that N losses via NO3- leaching or dissolved organic N loss to streams in  tropical systems can be high, too. And N2O is just one of the gaseous fluxes of N. Denitrification also produces N2, which is nearly impossible to measure.

Are tropical systems losing a greater proportion of their N via gaseous pathways? That part has never been quantified directly.

There is enough evidence out there to at least question the traditional view of the fractionating loss hypothesis driving global patterns in soil 15N, if not our views of the N cycle in the hot, cold, wet, and dry.

The next question is whether the processing hypothesis can explain more variation with fewer mechanisms. 

If so, global patterns of N cycling need to be reconsidered.

Thursday, September 20, 2012

Solving the riddle of the Amazon's nitrogen cycle

Sand vs. clay content (averaged 0.1° latitude/longitude) for the global soil 15N data set (so far). Red points are the Amazon. The one high blue point is from Panama.

When examining all the soil nitrogen isotope data from around the world, the Amazon rainforests always stood out as being too enriched based on everything else we knew about it. The Amazon is hotter and wetter than most other places, but it's del15N of soil organic matter was still 3‰ too high.

Something was different about the Amazon rain forests. 

There was either more gaseous N loss coming out of there than expected or more microbial processing that was enriching the soils. 

But what was it?

I looked at soil pH. Nothing unique there.

Soil carbon and nitrogen. Still couldn't explain the Amazon effect away.

One "outlier" for the Amazon has always been the white sands forests. Their 15N was never as enriched and those forests were always considered "nutrient poor".

Here's what Quesada et al. 2010 recently wrote on the topic: 

"That nitrogen is in excess for most tropical ecosystems (except forests growing on white sands) is, of course, already widely accepted, but from our pedogenic viewpoint, however, we also argue that as these losses continue to occur, the soil C:N ratio of the soils should also gradually increase (Fig. 12c) until a critical threshold around 30 mg kg−1 is reached. Beyond this, the system once again becomes more closed with respect to the nitrogen cycle, and thus enrichment ceases and the soil _15N tends back towards the isotopic composition of the input precipitation (ca. 0‰). The white sands forests of Amazonia have long been known to have relatively depleted _15N (Martinelli et al., 1999), and a large fraction of the sites on the “downside” of the curve are indeed sandy soils. But importantly, there are also other soils types with similar low P levels on the low side of the “breakpoint” (Fig. 11). This suggests that rather than just being a soil type effect, extremely low soil P concentrations may itself be the cause of these soils having strongly depleted _15N, with the phosphorus shortage itself leading to a lower rate of nitrogen return to soil. That is to say (in simplistic terms) at very low P availability, the forests actually become nitrogen limited."

When I look at the data, the one thing that stands out about the Amazon is the high clay content.

There just are few places in the world with such high clay concentrations. 

The white sands of the eastern Amazon might be the outlier for the Amazon, but it's the "black clays" of the western Amazon that are the outlier globally.

Quesada's argument about C:N and P might have some validity (I can work through that later), but the once you take into account clay concentrations, the Amazon effect almost disappears (<1 average="average" enrichment="enrichment">

1‰ is tolerable.

So how clay impacts soil 15N will be important. Does it control P availability and decomposition patterns that impact gaseous N loss? 

Or is it by impacting retention of enriched substrates and microbial processing?

Answering this question will get at whether Amazonian rainforests have a unique N cycle or not, but we at least now a proximal driver.

Wednesday, September 19, 2012

Beginning to reinterpret global soil N cycling patterns

If there is a state-change in how we think about global N cycling, or at least interpret soil 15N, it's likely to come by looking at covariates. For example, it's been hypothesized that hot sites have higher 15N because they have lower soil P, or higher soil pH, than cold sites, which is more directly driving large-scale patterns.

Or it's something else we haven't considered yet.

Working through the older literature on soil 15N, one paper that stands out is Knute Nadelhoffer and Bryan Fry's 1988 paper. There, they sampled a long-term experiment that varied litter inputs to soils at the University of Madison Arboretum. They took the soils and incubated them for 600 d, periodically leaching the soils.

Their main graph shows two things happen during incubation as microbes processed the soil. N concentrations declined and 15N went up.

I regraphed their data using %C instead of %N and you see something similar. Over time, C is being respired, C concentrations drop, and 15N of the SOM goes up.

About 80% of the N that was lost was from inorganic N in leachate. The other 20% was presumably from gaseous N loss.

The general idea that microbial processing of organic matter enriching 15N of the remaining material and causing C and N concentrations to decline has been shown repeatedly. Litter bag studies (Connin et al. 2001) show the same pattern. So do studies of different fractions of soil organic matter that differ in their degree of microbial processing (Kramer et al 2003):

The microbial processing concept has been applied to understanding vertical patterns in soil 15N, but never geographic patterns. 

It's possible that hot, dry sites are not (potentially) enriched in 15N because they lose a greater fraction of N to gaseous N loss, but instead because their soil organic matter is more decomposed.

To test for this, the key would be to look at soil C or N concentrations. C:N is generally considered an index of decomposition, but Nadelhoffer and Fry showed that as decomposition proceeded, both C and N declined. C concentration (or maybe N concentration) might be a better (not perfect) index of microbial processing. 

If the processing hypothesis predominates, then hot, dry sites would have lower %C and higher 15N. After accounting for variations in %C, if mean annual temperature or precipitation no longer predict soil 15N, this might be a good indication that they impact the degree of organic matter processing more than the relative importance of fractionating losses.

Once you get to the point of competing hypotheses, the only thing left to do is test them. 

Monday, September 17, 2012

Global soil 15N: the most recent synthesis was 10 years ago

Soil nitrogen isotopes have the potential to elucidate long-term patterns of N cycling. In short, the ratio of 15N/14N in soil organic matter should differentiate soils that lose more N through fractionating pathways like gaseous N loss vs. those that primarily lose N through non-fractionating pathways such as organic N loss or NO3- leaching.

In 1999, there were two major syntheses that were at odds. Handley's synthesis stated that high precipitation sites had low soil 15N--except it wasn't significant. They did show good relationships with latitude. Martinelli showed that tropical forests differed in soil 15N from temperate forests, which again highlights the importance of latitude.

The only problem is that the two papers showed different results. Handley had low-latitude soils with lower 15N, Martinelli higher.

Taken at face value, relative importance of denitrification should be higher in the temperate systems if one follows the Handley data, tropical systems for Martinelli.

A few years later, in 2003, Amundson et al. conducted a new synthesis. Like Handley, the data were global and across all ecosystem types. They examined soil 15N to 10 cm and 50 cm. They also calculated "regional" averages, which diminished the potential "pseudo replication".

The synthesis regressions, shown above seemed to have solved the confusion. Latitude wasn't the driver of soil 15N, it was climate. Hot sites had high soil 15N. So did dry sites.

From this, they concluded,

"Because most undisturbed soils are near N steady state, the observations suggest that an increasing fraction of ecosystem N losses are 15N-depleted forms (NO3, N2O, etc.) with decreasing MAP and increasing MAT. Wetter and colder ecosystems appear to be more efficient in conserving and recycling
mineral N."

The paper seemed to calm the waters on patterns and interpretations. Handley's earlier results on precipitation were supported. The latitude question was resolved. Interpretations were based on careful modeling of isotopic dynamics.

Or not. 

A few problems.

First, there were still no data that supported their interpretations that low soil 15N was associated with "efficient" conservation and recycling--the "openness" argument from earlier. They should have said that cold, wet systems lose a smaller fraction of N through fractionating pathways like gaseous N loss. The N cycle could still be "open" and lose a lot of N relative to rates of cycling, just lose it through DON or NO3- for example. 

Second, they still hadn't shown that precipitation had significantly impacted soil 15N. The P value for the 10-cm soil 15N samples was 0.14. I reanalyzed their data here:

For 50 cm, the P value was 0.09. Still hardly definitive.

For global syntheses, the number of soils examined was still incredibly small. For 0-10 cm, just 85 sites. For 0-50 cm, just 47. Remember, in 1978, Shearer et al. had done over 100 soils from the US alone. 

The lack of replication isn't a personal fault of the authors--although they could have asked Georgia and Danny for their raw data**. As a discipline, although there had been major questions about global patterns of N cycling, there was never a global effort to nail them down.

**Apparently no one ever asked them for their data. Danny recently wrote me "Although I was not certain, it turns out that I disposed of all of the raw data when my office was moved recently.  You, of course, have access to the paper. I'm afraid that is all there is. I never thought for one instance that anyone would ever be interested in those original data. I am sorry that I cannot be more helpful and sorry that our tediously acquired data will not be part of your data base."

The reason that the low replication is important is that the results are still highly sensitive to a few points. If I exclude 3 points from the regression, MAT is not significant.

So, where does that leave us? 

1) No one has yet to show that high precipitation sites would differ inherently in long-term N cycling characteristics than low-precipitation sites.

2) Hot sites have been shown to have significantly higher soil 15N than cold sites, but it's tenuous.

3) The interpretations of soil 15N are still shaky. Even accepting the conventional wisdom on how to interpret soil 15N, what these patterns implicate about the N cycle have not yet been resolved.

Lastly, there is one more thing that is conspicuously absent from all of these syntheses:


The C and N cycles are tightly linked, but the syntheses have been done in absence of understanding carbon.

In a bit, I'll show that also looking at carbon has the potential to fundamentally change our interpretations of global N cycling.

Sunday, September 16, 2012

N cycling 1999: tropics and temperate on its head

In 1999, two papers were published that began to frame global patterns of soil 15N. One was Handley's. Although they highlighted precipitation, their major significant pattern was latitude.

Martinelli et al also published a paper on global patterns of soil 15N in 1999. Like Handley, they, too, highlighted the importance of latitude. But for one detail, they were exactly the same. The best descriptor for the two results?


Martinelli compared ecosystems latitudinally by comparing temperate and tropical forests.

The authors initial statements were rooted in the idea that tropical forests are less N limited than temperate forests:

--"A number of lines of evidence suggest that N in most tropical forests is relatively more available than is N in most temperate forests. "

--"On average, more N circulates annually through lowland tropical forests, and does so at higher concentrations, than through temperate forests."

--"Emissions of N-containing trace gases are also higher, both absolutely and as a fraction of
N circulating through forests"

--"Comparable data on rates of N mineralization and leaching losses are sparser, but they generally show greater rates of N cycling and loss in many lowland tropical forests."

--"Overall, these observations suggest that N functions as an excess nutrient in most tropical forests, but not in the majority of temperate forests."

There were exceptions to these patterns such as tropical white-sand soils and montane forests and temperate forests dominated by N2-fixing trees or with high anthropogenic N deposition. But the initial premise was that N was more limiting in temperate than tropical soils, causing less N to be lost through fractionating pathways.

Like Handley, Martinelli et al.'s explanations were based on work that Vitousek had been associated with. And again, the authors talk about the "openness" of the N cycle, with open N cycles losing more N through gaseous pathways.

But why the difference?

One point is that Martinelli's tropical systems were primarily from Brazil. Handley's were from  Australia and Africa.

Could the nitrogen cycle just work differently in tropical South America than the other two continents?

Which was the right pattern? Remembering Shearer's earlier work from the US that showed an average soil 15N of +9‰, did the tropics actually have higher soil 15N than temperate ecosystems? Or were they the same?

And why did the different patterns exist?

A paper a few years later would seem to provide the definitive summary of soil 15N patterns, though the why question would linger.

Understanding global N cycling patterns circa 1999: precipitation is (not) important

As soil 15N measurements accumulated, interpreting the characteristics of the N cycle that generated variation in del 15N at broad scales began to develop.

In 1999, two papers were published that began to interpret 15N signatures of soil in terms of N cycle dynamics.

The first was by Linda Handley and others, "The 15N natural abundance (d15N) of ecosystem samples reflects measures of water availability".

With a title like that, you'd think the main conclusion would be simple.

Not so.

For soils at least, the authors showed strong relationships with latitude (shown above). Relationships with precipitation existed for foliar del15N, but not soils. Although their abstract reads "“The delta15N of whole soil ...when regressed on latitude and rainfall, provided the best model of these data, accounting for 49% of the variation in whole soil delta15N.” Yet, in the text they state that their model that predicted soil 15N with latitude and precipitation "was improved by deletion of rainfall as a model variable." 

Precipitation was not a significant predictor of soil 15N, despite the title and the abstract.

Still, the authors showed that tropical soils were depleted in 15N relative to high-latitude soils. 

The authors explained these patterns based on reasoning from Austin and Vitousek 1998: openness of the N cycle.

The more important inputs and outputs relative to internal cycling, the greater the del15N.

Whether precipitation was or wasn't important would have to wait to further syntheses.

The other paper published in 1999 also drew heavily from the work from Austin and Vitousek and also showed latitudinal gradients of 15N.

Yet, their interpretations were just the opposite.

Steps to understanding global patterns in N cycling

In the progression of our understanding of global patterns of N cycling, 1999 was a big year. Two papers were published that year that began to shape our interpretations about how geographic variations in climate impacted N cycling. They did so by examining broad patterns of nitrogen isotopes in soils and leaves.

Prior to 1999, Georgia Shearer and Danny Kohl had laid out the broadest patterns of nitrogen isotopes in soils, or lack thereof. Georgia had passed away recently, and her story is worth reading. Even though she never had received a PhD, was one of the world's experts in understanding nitrogen isotopes. Danny recently explained to me:

"As I recall, we undertook this study in part in response to a paper from Bremner's lab. They reported that half of the soils they measured had a Delta 15N value below zero and half above. We had reason to be skeptical of the accuracy of the reported data, so we undertook this much larger study...However, we had a hard time thinking of a mechanism that would result in negative values of 15N in soil N) since loss mechanism tend to favor the lighter isotope, resulting in the remaining N having a delta 15N value greater than zero."

The paper that they were looking at was published in Science in 1964. When they looked at the theory, they knew that N comes in to ecosystems with a signature of 0‰ relative to the atmosphere. All the processes known leave behind N enriched in 15N, not depleted. So how could any soils be depleted?

In response, they had collected over 100 soils from 20 US states and looked at the relationships between soil 15N and climate, depth, soil pH, and land use.

The major patterns?

There weren't any.

Soil depth patterns "were not consistent".
Differences among "cropland, pasture,  uncultivated land, and forest...were not striking".
N fertilization had "no systemic effect".

In short, there was a mean (9.2‰) and a range (90% fell between 5 and 12‰)

The take-home-message was that there was little pattern to soil 15N, at least in the US.

Looking for understanding of N cycling? Look elsewhere.

Curiously, their summary stated "less than half of the variation among soils in del15N of the total N could be accounted for by differences in environmental variables or soil characteristics."

Sometimes, though, less than half is more than we had before.

What patterns did they see?

According to their correlations, soils with high del15N came from wet, hot places with high pH, low sand, high clay. And soils with high N content.

Their approach to determining the correlations was not multivariate, but their were hints that soil 15N could be used to understand broad scale patterns in N cycling.

Unfortunately, that paper led to a 20-year drought in advance. Researchers afterwards focussed on using plant 15N as an index of recently fixed N. And it took about 20 years to realize that it didn't work that well.

The shift in approach to understanding 15N came about 21 years after with the publication of work by Martinelli et al. and Handley et al. These two papers offered different views about the major  controls on N cycling that are still reverberating. More on this soon.

Sunday, September 2, 2012

Quote from Shearer et al. 1978.

How much progress has their been in 35 years?

Shearer, G., D. H. Kohl, and S. H. Chien. 1978. N-15 Abundance In A Wide Variety Of Soils. Soil Science Society of America Journal 42:899-902.